Effects of dietary soybean meal and photoperiod cycle on osmoregulation following seawater exposure in Atlantic salmon smolts

Journal of Fish Biology

Volumn 69, Issue 5, 2006, Pages 1396-1426

  Bakke McKellep, A M ^a   Refstie, S ^a,b   Stefansson, S O ^c   Vanthanouvong, V ^d   Roomans, G ^d   Hemre, G I ^e   Krogdahl, A ^a  

^a NORWEGIAN UNIVERSITY OF LIFE SCIENCES   (Norway)

^b NOFIMA   (Norway)

^c UNIVERSITY OF BERGEN   (Norway)

^d UPPSALA UNIVERSITY   (Sweden)

^e INSTITUTE OF MARINE RESEARCH   (Norway)

Author keywords

Digestive enzymes; Histology; Ion concentration; Na+ K + ATPase; Osmolality; X ray microanalysis

Indexed keywords

DIET; ENZYME ACTIVITY; HISTOLOGY; JUVENILE; OSMOREGULATION; PHOTOPERIOD; SALINITY; SALMONID; SEAWATER; SMOLT; SOYBEAN;

ATLANTIC OCEAN;

GLYCINE MAX; SALMO SALAR;

EID: 33750621545     PISSN: 00221112     EISSN: 10958649     Source Type: Journal    
DOI: 10.1111/j.1095-8649.2006.01201.x     Document Type: Article

References (62)

1. Arnesen, A. M., Toften, H., Agustsson, T., Stefansson, S. O., Handeland, S. O. & Björnsson, T. (2003). Osmoregulation, feed intake, growth and growth hormone levels in 0+ Atlantic salmon (Salmo salar L.) transferred to seawater at different stages of smolt development. Aquaculture 222, 167-187.
2. Baeverfjord, G. & Krogdahl, Å. (1996). Development and regression of soybean meal induced enteritis in Atlantic salmon, Salmo salar L., distal intestine: a comparison with the intestines of fasted fish. Journal of Fish Diseases 19, 375-387.
3. Bakke-McKellep, A. M., Press, C. M., Baeverfjord, G., Krogdahl, Å. & Landsverk, T. (2000). Changes in immune and enzyme histochemical phenotypes of cells in the intestinal mucosa of Atlantic salmon, Salmo salar L., with soybean meal-induced enteritis. Journal of Fish Diseases 23, 115-127.
4. Björnsson, B. T., Thorarensen, H., Ogasawara, T. & Kristinsson, J. B. (1989). Photoperiod and temperature affect plasma growth hormone levels, growth condition factor and hypoosmoregulatory ability of juvenile Atlantic salmon (Salmo salar) during parr-smolt transformation. Aquaculture 82, 77-91.
5. Cameron, I. L. & Smith, N. K. R. (1980). Energy dispersive X-ray microanalysis of the concentration of elements in relation to cell reproduction in normal and in cancer cells. Scanning Electron Microscopy 1980/II, 463-474.
6. Cutler, C. P. & Cramb, G. (2001). Molecular physiology of osmoregulation in eels and other teleosts: the role of transporter isoforms and gene duplication. Comparative Biochemistry and Physiology 130A, 551-564.
7. Dahlquist, A. (1970). Assay of intestinal disaccharidases. Enzymologia Biologica et Clinica 11, 52-66.
8. D'Cotta, H., Valotaire, C., le Gac, F. & Prunet, P. (2000). Synthesis of gill Na(+)-K(+)-ATPase in Atlantic salmon smolts: differences in alpha-mRNA and alpha-protein levels. American Journal of Physiology 278, R101-R110.
9. Dragomir, A. & Roomans, G. M. (2000). X-ray microanalysis of intestinal chloride transport in vitro and in vivo. Microscopy Research and Technique 50, 176-181.
10. Duncan, N. J. & Bromage, N. (1998). The effect of different periods of constant short days on smoltification in juvenile Atlantic salmon (Salmo salar). Aquaculture 168, 369-386.
11. FAO (2003). Review of the state of world aquaculture. FAO Fisheries Circular 886.
12. Francis, G., Makkar, H. P. S. & Becker, K. (2001). Antinutritional factors present in plant-derived alternate fish feed ingredients and their effects in fish. Aquaculture 199, 197-227.
13. Grundin, T. G., Roomans, G. M., Forslind, B., Lindberg, M. & Werner, Y. (1985). X-ray microanalysis of psoriatic skin. Journal of Investigative Dermatology 85, 378-380.
14. Halm, D. R. & Rick, R. (1992). Secretion of K and Cl across colonic epithelium: cellular localization using electron microprobe analysis. American Journal of Physiology 262, C1392-C1402.
15. Handeland, S. O. & Stefansson, S. O. (2001). Photoperiod control and influence of body size on off-season parr-smolt transformation and post-smolt growth. Aquaculture 192, 291-307.
16. Handeland, S. O. & Stefansson, S. O. (2002). Effects of salinity acclimation on pre-smolt growth, smolting and post-smolt performance in off-season Atlantic salmon smolts (Salmo salar L.). Aquaculture 209, 125-137.
17. Handeland, S. O., Berge, Å., Björnsson, B. T., Lie, Ø. & Stefansson, S. O. (2000). Seawater adaptation by out-of-season Atlantic salmon (Salmo salar L.) smolts at different temperatures. Aquaculture 181, 377-396.
18. Handeland, S. O., Wilkinson, E., Sveinsbø, B., McCormick, S. D. & Stefansson, S. O. (2004). Temperature influence on the development and loss of seawater tolerance in two fast-growing strains of Atlantic salmon. Aquaculture 233, 513-529.
19. Hardy, R. W. (1996). Alternate protein sources for salmon and trout diets. Animal Feed Science and Technology 59, 71-80.
20. van den Ingh, T. S. G. A. M., Krogdahl, Å., Olli, J. J., Hendricks, H. G. C. J. M. & Koninkx, J. F. J. G. (1991). Effects of soybean containing diets on the proximal and distal intestine in Atlantic salmon (Salmo salar): a morphological study. Aquaculture 94, 297-305.
21. Kaushik, S. J., Cravedi, J. P., Lalles, J. P., Sumpter, J., Fauconneau, B. & Laroche, M. (1995). Partial or total replacement of fish meal by soybean protein on growth, protein utilization, potential estrogenic or antigenic effects, cholesterolemia and flesh quality in rainbow trout, Oncorhynchus mykiss. Aquaculture 133, 257-274.
22. Kirsch, R., Humbert, W. & Simonneaux, V. (1985). The gut as an osmoregulatory organ: comparative aspects and special references to fishes. In Transport Processes, Iono- and Osmoregulation (Gilles, R. & Gilles-Baillien, M., eds), pp. 265-277. Berlin: Springer Verlag.
23. Krogdahl, Å., Bakke-McKellep, A. M., Røed, K. H. & Baeverfjord, G. (2000). Feeding Atlantic salmon Salmo salar L. soybean products: effects on disease resistance (furunculosis), and lysozyme and IgM levels in the intestinal mucosa. Aquaculture Nutrition 6, 77-84.
24. Krogdahl, Å., Bakke-McKellep, A. M. & Baeverfjord, G. (2003). Effects of graded levels of standard soybean meal on intestinal structure, mucosal enzyme activities, and pancreatic response in Atlantic salmon (Salmo salar L.). Aquaculture Nutrition 9, 361-371.
25. +/glucose cotransporter. Proceedings of the National Academy of Sciences of the USA 93, 13367-13370.
26. Loretz, C. A. (1995). Electrophysiology of ion transport in teleost intestinal cells. In Fish Physiology, Vol. 14 (Wood, C. M. & Shuttleworth, T. J., eds), pp. 25-56. San Diego, CA: Academic Press.
27. Marshall, W. S., Howard, J. A., Cozzi, R. R. F. & Lynch, E. M. (2002). NaCl and fluid secretion by the intestine of the teleost Fundulus heteroclitus: involvement of CFTR. Journal of Experimental Biology 205, 745-758.
28. +-ATPase activity. Canadian Journal of Fisheries and Aquatic Sciences 50, 656-658.
29. +-ATPase in Atlantic salmon (Salmo salar): interaction with cortisol. General and Comparative Endocrinology 101, 3-11.
30. +/glucose cotransporter is a molecular water pump. Journal of Physiology 508, 15-21.
31. Naylor, R. L., Goldburg, R. J., Primavera, J. H., Kautsky, N., Beveridge, M. C. M., Clay, J., Folke, C., Lubchenco, J., Mooney, H. & Troell, M. (2000). Effect of aquaculture on world fish supplies. Nature 405, 1017-1024.
32. Nordrum, S., Bakke-McKellep, A. M., Krogdahl, Å. & Buddington, R. K. (2000). Effects of soybean meal and salinity on intestinal transport of nutrients in Atlantic salmon (Salmo salar L.) and rainbow trout (Oncorhynchus mykiss). Comparative Biochemistry and Physiology 125B, 317-335.
33. Oliva-Teles, A., Gouveia, A. J., Gomes, E. & Rema, P. (1994). The effect of different processing treatments on soybean meal utilization by rainbow trout, Oncorhynchus mykiss. Aquaculture 124, 343-349.
34. Olli, J. & Krogdahl, Å. (1994). Nutritive value of four soybean products as protein sources in diets for rainbow trout (Oncorhynchus mykiss, Walbaum) reared in fresh water. Acta Agriculturae Scandinavica A 44, 185-192.
35. Olli, J. & Krogdahl, Å. (1995). Alcohol soluble components of soybean seem to reduce lipid digestibility in fish-meal-based diets for Atlantic salmon, Salmo salar L. Aquaculture Research 26, 831-835.
36. Olli, J., Krogdahl, Å., van den Ingh, T. S. G. A. M. & Brattås, L. E. (1994). Nutritive value of four soybean products in diets for Atlantic salmon (Salmo salar, L.). Acta Agriculturae Scandinavica A 44, 50-60.
37. O'Loughlin, E. V., Hunt, D. M., Bostrom, T. E., Hunter, D., Gaskin, K. J., Gyory, A. & Cockayne, D. J. (1996). X-ray microanalysis of cell elements in normal and cystic fibrosis jejunum: evidence for chloride secretion in villi. Gastroenterology 110, 411-418.
38. Refstie, S., Helland, S. & Storebakken, T. (1997). Adaptation to soybean meal in diets for rainbow trout, Oncorhynchus mykiss. Aquaculture 153, 263-272.
39. Refstie, S., Storebakken, T. & Roem, A. J. (1998). Feed consumption and conversion in Atlantic salmon (Salmo salar) fed diets with fish meal, extracted soybean meal or soybean meal with reduced content of oligosaccharides, trypsin inhibitors, lectins and soya antigens. Aquaculture 162, 301-312.
40. Refstie, S., Korsøen, Ø. J., Storebakken, T., Baeverfjord, G., Lein, I. & Roem, A. J. (2000). Differing nutritional responses to dietary defatted soybean meal in rainbow trout (Oncorhynchus mykiss) and Atlantic salmon (Salmo salar). Aquaculture 190, 49-63.
41. Refstie, S., Storebakken, T., Baeverfjord, G. & Roem, A. J. (2001). Long-term protein and lipid growth of Atlantic salmon (Salmo salar) fed diets with partial replacement of fish meal by soy protein products at medium or high lipid level. Aquaculture 193, 91-106.
42. Refstie, S., Sahlström, S., Bråthen, E., Baeverfjord, G. & Krogedal, P. (2005). Lactic acid fermentation eliminates indigestible carbohydrates and antinutritional factors in soybean meal for Atlantic salmon (Salmo salar). Aquaculture 246, 331-345.
43. Roomans, G. M. (1988). Quantitative X-ray microanalysis of biological specimens. Journal of Electron Microscopy Technique 9, 19-44.
44. Rumsey, G. L., Endres, J. G., Bowser, P. R., Earnest-Koons, K. A., Anderson, D. P. & Siwicki, A. K. (1994a). Soy protein in diets of rainbow trout: effects on growth, protein absorption, gastrointestinal histology, and non-specific serologic and immune response. In Nutrition and Utilization Technology in Aquaculture (Lim, C. & Sessa, D. J., eds), pp. 166-188. Champaign, IL: AOAC Press.
45. Rumsey, G. L., Siwicki, A. K., Anderson, D. P. & Bowser, P. R. (1994b). Effect of soybean protein on serological response, nonspecific defense mechanisms, growth, and protein utilization in rainbow trout. Veterinary Immunology and Immunopathology 41, 323-339.
46. SAS (1989). SAS/STAT User's Guide. Cary, NC: SAS Institute Inc.
47. Sanden, M., Berntssen, M. H. G., Krogdahl, Å., Hemre, G.-I. & Bakke-McKellep, A. M. (2005a). An examination of the intestinal tract of Atlantic salmon (Salmo salar L.) parr fed different varieties of soy and maize. Journal of Fish Diseases 28, 317-330.
48. Sanden, M., Krogdahl, Å., Bakke-McKellep, A. M., Buddington, R. K., Hemre, G.-I. (2005b). Growth, organ development and function of Atlantic salmon, Salmo salar L. parr fed genetically modified (GM) soybeans and maize. Aquaculture Nutrition 12, 1-14.
49. +-ATPase in gills and pyloric caeca of brown trout (Salmo trutta) during acclimation to seawater. Physiological and Biochemical Zoology 73, 446-453.
50. Sigholt, T., Staurnes, M., Jakobsen, H. J. & Åsgård, T. (1995). Effects of continuous light and long-winter photoperiod on smolting, seawater survival and growth in Atlantic salmon (Salmo salar). Aquaculture 130, 373-388.
51. Sigholt, T., Åsgård, T. & Staurnes, M. (1998). Timing of parr-smolt transformation in Atlantic salmon (Salmo salar): effects of changes in temperature and photoperiod. Aquaculture 160, 129-144.
52. Skilbrei, O. T. & Hansen, T. (2004). Effects of pre-smolt photoperiod regimes on postsmolt growth rates of different genetic groups of Atlantic salmon (Salmo salar). Aquaculture 242, 671-688.
53. Stoldt, W. (1952). Vorschlag zur Vereinheitlichung der Fettbestimmung in Lebensmitteln. Fette, Seifen, Anstrichmittel 54, 206-207.
54. Sundell, K., Jutfelt, F., Ágústsson, T., Olsen, R. E., Sandblom, E., Hansen, T. & Björnsson, B. T. (2003). Intestinal transport mechanisms and plasma cortisol levels during normal and out-of-season parr-smolt transformation of Atlantic salmon, Salmo salar. Aquaculture 222, 265-285.
55. Tacon, A. G. J., Haastler, J. V., Featherstone, P. B., Kerr, K. & Jackson, A. J. (1983). Studies on the utilization of full-fat and solvent extracted soybean meal in a complete diet for rainbow trout. Nippon Suisan Gakkaishi 49, 1437-1443.
56. Tietz, N. W. (1995). Clinical Guide to Laboratory Tests, 3rd edn. Philadelphia, PA: WB Saunders Company.
57. Vanthanouvong, V., Högman, M. & Roomans, G. M. (2003). In vitro and in situ experimental models for X-ray microanalysis of intestinal epithelium. Microscopy Research and Technique 62, 211-217.
58. Viellette, P. A., White, R. J. & Specker, J. L. (1993). Changes in intestinal fluid transport in Atlantic salmon (Salmo salar L.) during parr-smolt transformation. Fish Physiology and Biochemistry 12, 193-202.
59. Villarreal, C. A., Thorpe, J. E. & Miles, M. S. (1988). Influence of photoperiod on growth changes in juvenile Atlantic salmon (Salmo salar). Journal of Fish Biology 33, 15-30.
60. Wróblewski, R., Roomans, G. M., Jansson, E. & Edström, L. (1978). Electron probe X-ray microanalysis of human muscle biopsies. Histochemistry 55, 281-292.
61. Zaugg, W. S. (1982). A simplified preparation for adenosine triphosphatase determination in gill tissue. Canadian Journal of Fisheries and Aquatic Sciences 39, 215-217.
62. von Zglinicki, T. & Roomans, G. M. (1993). Water and ion shifts in mouse intestinal cells following VIP stimulation. Epithelial Cell Biology 2, 143-149.