Ionoregulatory physiology of two species of African lungfishes Protopterus dolloi and Protopterus annectens

Journal of Fish Biology

Volumn 75, Issue 4, 2009, Pages 862-884

  Patel, M ^a   Iftikar, F I ^b   Leonard, E M ^b   Ip, Y K ^c   Wood, C M ^b  

^a UNIVERSITY OF TORONTO   (Canada)

^b MCMASTER UNIVERSITY   (Canada)

^c NATIONAL UNIVERSITY OF SINGAPORE   (Singapore)

Author keywords

Calcium; Chloride; Feeding; Ion fluxes; Sodium; Terrestrialization

Indexed keywords

CALCIUM; CHLORIDE; SODIUM;

ANIMAL; ARTICLE; BLOOD; DIET; ELECTROLYTE BALANCE; FISH; PHYSIOLOGY; URINE;

ANIMALS; CALCIUM; CHLORIDES; DIET; FISHES; SODIUM; WATER-ELECTROLYTE BALANCE;

GLYCERIDAE; PROTOPTERIDAE; PROTOPTERUS; PROTOPTERUS ANNECTENS; PROTOPTERUS DOLLOI; TELEOSTEI;

EID: 70349332985     PISSN: 00221112     EISSN: 10958649     Source Type: Journal    
DOI: 10.1111/j.1095-8649.2009.02335.x     Document Type: Article

References (62)

1. Abbink, W., Bevelander, G. S., Rotllant, J., Canario, A. V. M. & Flik, G. (2004). Calcium handling in Sparus auratus: effects of water and dietary calcium levels on mineral composition, cortisol and PTHrP levels. Journal of Experimental Biology 207, 4077 4084.
2. Babiker, M. M. & Rankin, J. C. (1979). Renal and vascular effects of neurohypophysial hormones in the African lungfish Protopterus annectens. General and Comparative Endocrinology 37, 26 34.
3. Boisen, A. M., Amstrup, J., Novak, I. & Grosell, M. (2003). Sodium and chloride transport in soft water and hard water acclimated zebrafish (Danio rerio). Biochimica et Biophysica Acta 1618, 207 218.
4. +) during digestion: implications for homeostatic balance in freshwater rainbow trout. American Journal of Physiology R 291, 1764 1772.
5. 2+ during the digestion of a single meal in the freshwater rainbow trout. Journal of Comparative Physiology B 177, 349 360.
6. Chew, S. F., Ong, T. F., Ho, L., Tam, W. L., Loong, A. M. & Hiong, K. C. (2003). Urea synthesis in the African lungfish (Protopterus dolloi): hepatic carbamoyl phosphate synthetase III and glutamine synthetase are upregulated by 6 days of aerial exposure. Journal of Experimental Biology 206, 3615 3624.
7. Chew, S. F., Chan, N. K. Y., Loong, A. M. Hiong, K. C., Tam, W. L. & Ip, Y. K. (2004). Nitrogen metabolism in the African lungfish (Protopterus dolloi) aestivating in a mucus cocoon on land. Journal of Experimental Biology 207, 777 786.
8. Curtis, B. J. & Wood, C. M. (1991). The function of the urinary bladder in vivo in the freshwater rainbow trout. Journal of Experimental Biology 155, 567 583.
9. DeLaney, R. G., Lahiri, S., Fishman, A. P. (1974). Aestivation of the African lungfish Protopterus aethiopicus: cardiovascular and respiratory functions. Journal of Experimental Biology 61, 111 128.
10. DeLaney, R. G., Lahiri, S., Hamilton, R. & Fishman, A. P. (1977). Acid base balance and plasma composition in the aestivating lungfish (Protopterus). American Journal of Physiology 232, 10 17.
11. Evans, D. H., Piermarini, P. M. & Choe, K. P. (2005). The multifunctional fish gill: dominant site of gas exchange, osmoregulation, acid-base regulation, and excretion of nitrogenous waste. Physiological Reviews 85, 97 177.
12. Fishman, A. P., Pack, A. I., DeLaney, R. G. & Galante, R. J. (1986). Estivation in Protopterus. Journal of Morphology Supplement 1, 237 248.
13. Flik, G., Fenwick, J. C., Kolar, Z., Mayer-Gostan, N. & Wendelar Bonga, S. E. (1986). Effects of ovine prolactin on calcium uptake and distribution in Oreochromis mossambicus. American Journal of Physiology R 250, 161 166.
14. Galvez, F., Reid, S. D., Hawkings, G. & Goss, G. G. (2002). Isolation and characterization of mithochondria-rich cell types from the gill of freshwater rainbow trout. American Journal of Physiology R 282, 658 668.
15. Galvez, F., Wong, D. & Wood, C. M. (2006). Cadmium and calcium uptake in isolated mitochondria-rich cell populations from the gills of the freshwater rainbow trout. American Journal of Physiology R 291, 170 176.
16. Gilmour, K. M., Euverman, R. M., Esbaugh, A. J., Keeney, L., Chew, S. F., Ip, Y. K. & Perry, S. F. (2007). Mechanisms of acid-base regulation in the African lungfish Protopterus annectens. Journal of Experimental Biology 210, 1944 1959.
17. Gordon, M. S. (1959). Ionic regulation in the brown trout (Salmo trutta). Journal of Experimental Biology 36, 227 252.
18. Goss, G. G., Adamia, S. & Galvez, F. (2001). Peanut lectin binds to a subpopulation of mitochondria rich cells in the rainbow trout gill epithelium. American Journal of Physiology R 281, 1718 1725.
19. Greenaway, P. (1972). Calcium regulation in the freshwater crayfish Austropotamobius pallipes (Lereboullet). I. Calcium balance in the intermoult animal. Journal of Experimental Biology 57, 471 487.
20. Greenwood, P. H. (1986). The natural history of African lungfishes. In The Biology and Evolution of Lungfishes (Bemis, W. E., Burggren, W. W. & Kemp, N. E., eds), pp. 163 179. New York, NY : Alan R. Liss, Inc.
21. Hanssen, R. G., Lafeber, F. P., Flik, G., & Wendelaar Bonga, S. E. (1989). Ionic and total calcium levels in the blood of the European eel (Anguilla anguilla): effects of stanniectomy and hypocalcin replacement therapy. Journal of Experimental Biology 141, 177 186.
22. Hickman, C. & Trump, B. (1969). Kidney. In Fish Physiology, Vol. I (Hoar, W. S. & Randall, D. J., eds), pp. 150, 211 212. New York, NY : Academic Press, Inc.
23. Houston, A. H. & Koss, T. F. (1984). Plasma and red cell ionic composition in rainbow trout exposed to progressive temperature increases. Journal of Experimental Biology 110, 53 67.
24. Houston, A. H., Madden, J. A. & DeWilde, M. A. (1970). Environmental temperature and the body fluid system of the freshwater teleost - IV. Water-electrolyte regulation in thermally acclimated carp, Cyprinus carpio. Comparative Biochemistry and Physiology 34, 805 818.
25. Iftikar, F., Patel, M., Ip, Y. K. & Wood, C. M. (2008). The influence of feeding on aerial and aquatic oxygen consumption, nitrogenous waste excretion, and metabolic fuel usage in the African lungfish Protopterus annectens. Canadian Journal of Zoology 86, 790 800.
26. Janssens, P. A. (1963). The metabolism of the aestivating African lungfish. Comparative Biochemistry and Physiology 11, 105 117.
27. Janssens, P. A. & Cohen, P. P. (1966). Ornithine-urea cycle enzymes in the African lungfish Protopterus aethiopicus. Science 152, 358 359.
28. Johansen, K. (1970). Air-breathing in fishes. In Fish Physiology, Vol. 5 (Hoar, W. S. & Randall, D. J., eds), pp. 361 411. New York, NY : Academic Press, Inc.
29. Laurent, P. & Dunel, S. (1976). Functional organization of the teleost gill. I. Blood pathways. Acta Zoologica. (Stockhlom) 57, 189 209.
30. Laurent, P., DeLaney, R. G. & Fishman, A. P. (1978). The vasculature of the gills in the aquatic and aestivating lungfish (Protopterus aethiopicus). Journal of Morphology 158, 173 208.
31. 2+ transport by fish gills: retrospective review and prospective synthesis. Journal of Experimental Zoology 293, 264 283.
32. McCormick, S. D., Hasegawa, S. & Hirano, T. (1992). Calcium uptake in the skin of a freshwater teleost. Proceedings of the National Academy of Sciences 89, 3635 3638.
33. McMahon, B. (1970). The relative efficiency of gaseous exchange across the lungs and gills of an African lungfish Protopterus aethiopicus. Journal of Experimental Biology 52, 1 15.
34. Motais, R., Romeu, F. G. & Maetz, J. (1966). Exchange diffusion effect and euryhalinity in teleosts. Journal of General Physiology 50, 391 422.
35. O'Donnell, M. J. & Rheault, M. R. (2005). Ion-selective microelectrode analysis of salicylate transport by the Malpighian tubules and gut of Drosophila melanogaster. Journal of Experimental Biology 208, 93 104.
36. Odulye, S. O. (1977). Unidirectional water and sodium fluxes and respiratory metabolism in the African lung-fish, Protopterus annectens. Journal of Comparative Physiology 119, 127 139.
37. Pang, P. K., Pang, R. K., Liu, V. K. & Sokabe, H. (1981). Effect of fish angiotensins and angiotensin-like substances on killifish calcium regulation. General and Comparative Endocrinology 43, 292 298.
38. Patel, M., Iftikar, F., Smith, R., Ip, Y. K. & Wood, C. M. (2009). Water balance and kidney function in two species of African lungfish Protopterus dolloi and Protopterus annectens. Comparative Biochemistry and Physiology A 152, 149 157.
39. Perry, S. F. (1997). The chloride cell: structure and function in the gill of freshwater fishes. Annual Review of Physiology 59, 325 347.
40. Perry, S. F., Gilmour, K. M., Vulesevic, B., McNeill, B., Chew, S. F. & Ip, Y. K. 2005). Circulating catecholamines and cardiorespiratory responses in hypoxic lungfish (Protopterus dolloi): a comparison of aquatic and aerial hypoxia. Physiological and Biochemical Zoology 178, 7853 7865.
41. Pisam, M. & Rambourg, A. (1991). Mitochondria rich cells in the gill and epithelium of teleost fishes: an ultrastructural approach. International Review of Cytology 130, 191 232.
42. Pisam, M., Caroff, A. & Rambourg, A. (1987). Two types of chloride cells in the gill epithelium of a freshwater adapted euryhaline fish Lebistes reticulates; their modification during adaptation to seawater. American Journal of Anatomy 179, 40 50.
43. Pisam, M., Boeuf, G., Prunet, P. & Rambourg, A. (1990). Ultrastructural features of mitochondria rich cells in stenohaline freshwater and seawater fishes. American Journal of Anatomy 187, 21 31.
44. Pisam, M., Auperin, B., Prunet, P., Rentierdelrue, F., Martial, J. & Rambourg, A. (1993). Effects of prolactin on alpha chloride and beta chloride cells in the gill epithelium of the saltwater adapted tilapia Oreochromis niloticus. The Anatomical Record 235, 275 284.
45. Potts, W. T. W. & Fleming, W. R. (1970). The effects of prolactin and divalent ions on the permeability of water of Fundulus kansae. Journal of Experimental Biology 53, 317 327.
46. Rogers, J. T., Richards, J. G. & Wood, C. M. (2003). Ionoregulatory disruption as the acute toxic mechanism for lead in the rainbow torut (Oncorhynchus mykiss). Aquatic Toxicology 64, 215 234.
47. Sawyer, W. H., Uchiyama, M. & Pang, P. K. T. (1982). Control of renal functions in lungfishes. Federation of American Societies for Experimental Biology 41, 2361 2364.
48. Scott, G. R., Rogers, J. T., Richards, J. G., Wood, C. M. & Schulte, P. M. (2004). Intraspecific divergence of ionoregulatory physiology in the euryhaline teleost Fundulus heteroclitus: possible mechanisms of freshwater adaptation. Journal of Experimental Biology 207, 3399 3410.
49. Sharratt, B. M., Chester Jones, I. & Bellamy, D. (1964). Water and electrolyte composition of the body and renal function of the eel (Anguilla anguilla). Comparative Biochemistry and Physiology 11, 9 18.
50. Smith, H. (1930). Metabolism of the lungfish, Protopterus aethiopicus. Journal of Biological Chemistry 88, 97 130.
51. Smith, H. W. (1935). Lung-fish. Aquarium 1, 241 243.
52. Smith, N. F., Eddy, F. B. & Talbot, C. (1989). Dietary salt intake and its relevance to ionic regulation in freshwater salmonids. Journal of Fish Biology 35, 749 753.
53. Staples, J. F., Kajimura, M., Wood, C. M., Patel, M., Ip, Y. K. & McClelland, G. B. (2008). Enzymatic and mitochondrial responses to five months of aerial exposure in the slender lungfish (Protopterus dolloi). Journal of Fish Biology 73, 608 622.
54. Sturla, M., Masini, M. A., Prato, P., Grattarola, C. & Uva, B. (2001). Mitochondria rich cells in gills and skin of an African lungfish Protopterus annectans. Cell and Tissue Research 303, 351 358.
55. Takezaki, N., Figuero, F., Zaleska-Rutczynska, Z., Takahata, N. & Klein, J. (2004). The phylogenetic relationship of tetrapod, coelacanth, and lungfish revealed by the sequences of forty-four nuclear genes. Molecular Biology and Evolution 21, 1512 1524.
56. Urist, M. R., Uyeno, S., King, E., Okada, M. & Applegate, S. (1972). Calcium and phosphorus in the skeleton and blood of the lungfish Lepidosiren paradoxa, with comment on humoral factors in calcium homeostasis in the Osteichthyes. Comparative Biochemistry and Physiology A 42, 393 408.
57. Wilkie, M., Morgan, T., Galvez, F., Smith, R., Kajimura, M., Ip, Y. & Wood, C. M. (2007). The African lungfish (Protopterus dolloi); ionoregulation and osmoregulation in a fish out of water. Physiological and Biochemical Zoology 80, 99 112.
58. Wood, C. M. (1988). Acid-base and ionic exchanges at gills and kidney after exhaustive exercise in the rainbow trout. Journal of Experimental Biology 146, 461 481.
59. Wood, C. M., Walsh, P. J., Chew, S. F. & Ip, Y. K. (2005a). Greatly elevated urea excretion after air exposure appears to be carrier mediated in the slender lungfish (Protopterus dolloi). Physiological and Biochemical Zoology 78, 893 907.
60. Wood, C. M., Walsh, P. J., Chew, S. F. & Ip, Y. K. (2005b). Ammonia tolerance in the slender lungfish (Protopterus dolloi): the importance of environmental acidification. Canadian Journal of Zoology 83, 507 516.
61. Wright, P. (2007). Ionic, osmotic, and nitrogenous waste regulation. In Fish Physiology, Vol. 26 (McKenzie, D. J., Farrell, A. P. & Brauner, C. J., eds), pp. 283 319. New York NY : Academic Press, Inc.
62. Zall, D. M., Fischer, M. D. & Garner, Q. M. (1956). Photometric determination of chloride in water. Analytical Chemistry 28, 1665 1678.