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Digestive efficiency, free amino acid pools and quality of growth performance in Atlantic salmon (Salmo salar L.) affected by light regimes and vaccine types

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Abstract

This study comprised the results of three different seawater trials using unique combination of techniques to study protease digestive efficiency and growth performance quality to illustrate the effects of light regimes and vaccine types in Atlantic salmon (Salmo salar L.). Fish with higher growth had higher trypsin (T) and chymotrypsin (C) specific activities with higher T/C ratio or slope T/C ratio [calculated from the regression between trypsin (y) and chymotrypsin (x) specific activities] in the pyloric caeca. The T/C ratios indicated fish growth rates over a period of 1–2 months, while the slope T/C ratios indicated fish growth rates at sampling. Adaptation period for adjustment to the new environment of continuous light was 70 days, indicated by the differences in trypsin specific activities and the crossing of slope T/C ratio regressions following with the changes in growth rate directions between the control and the treated group. Vaccine types affected fish vertebral growth, and additional continuous light enhanced the impact of vaccines on fish growth during springtime, indicated by differences in slope T/C ratios. Continuous light stimulated fish growth during winter to spring, when the natural day length was short, without significantly changing white muscle and oocyte qualities in the fish of about 500 g, except for significantly increased white muscle RNA concentration. Continuous light also reduced fish growth rate later during summer, when the natural day length was long, by precedently decreasing the T/C ratio in late spring. Interestingly, plasma levels of free lysine related to tryptic digestion were correlated with trypsin specific activity levels. Continuous light caused higher levels of most free amino acids (FAA) involved in nitrogen metabolism, higher incorporation of essential FAA for protein synthesis, and higher protein turnover rate (free hydroxyproline levels) in both plasma and white muscle. However, continuous light did not affect higher protein content, intracellular buffering capacity and RNA levels in the white muscle of the fish of about 1 kg, probably due to limitation of FAA available for protein synthesis. It is therefore suggested that enhancing fish growth by continuous light stimulation should be accompanied by increasing availability or content of dietary protein (and probably minerals), which in turn would improve the quality of fish growth performance through increasing fillet protein concentration, strengthening vertebral growth, and delaying oocyte development.

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References

  • Ablett RF, Sinnhuber RO, Holmes RM, Selivon-chick DP (1981) The effect of prolonged administration of bovine insulin in rainbow trout (Salmo gairdneri R). Gen Comp Endocrinol 43:211–217

    Article  PubMed  CAS  Google Scholar 

  • Areekijseree M, Engkagul A, Kovitvadhi S, Kovitvadhi U, Thongpan A, Rungruangsak-Torrissen K (2006) Development of digestive enzymes and in vitro digestibility of different species of phytoplankton for culture of early juveniles of the freshwater pearl mussel, Hyriopsis (Hyriopsis) bialatus Simpson, 1900. Invertebr Reprod Dev 49:255–262

    CAS  Google Scholar 

  • Berg AE, Rødseth OM, Tangerås A, Hansen TJ (2006) Time of vaccination influences development of adherences, growth and spinal deformities in Atlantic salmon (Salmo salar L.). Dis Aquat Org 69:239–248

    Article  PubMed  Google Scholar 

  • Blier PU, Lemieux H, Devlin RH (2002) Is the growth rate of fish set by digestive enzymes or metabolic capacity of tissues? Insight from transgenic coho salmon. Aquaculture 209:379–384

    Article  CAS  Google Scholar 

  • Carter CG, Houlihan DF, Buchanan B, Mitchell AI (1993) Protein-nitrogen flux and protein growth efficiency of individual Atlantic salmon (Salmo salar L.). Fish Physiol Biochem 12:305–315

    Article  CAS  Google Scholar 

  • Cho CY (1992) Feeding systems for rainbow trout and other salmonids with reference to current estimates of energy and protein requirements. Aquaculture 100:107–123

    Article  Google Scholar 

  • Donaldson EM, Fagerlund UHM, Higgs DA, McBride JR (1979) Hormonal enhancement of growth. In: Hoar WS, Randall DJ, Brett RJ (eds) Fish physiology, vol 8. Academic Press, New York, USA, pp 455–579

    Google Scholar 

  • Espe M, Lied E, Torrissen KR (1993) In vitro protein synthesis in muscle of Atlantic salmon (Salmo salar) as affected by the degree of proteolysis in feeds. J Anim Physiol Anim Nutr 69:260–266

    Article  CAS  Google Scholar 

  • Fjelldal PG, Nordgarden U, Berg A, Grotmol S, Totland GK, Wargelius A, Hansen T (2005) Vertebrae of the trunk and tail display different growth rates in response to photoperiod in Atlantic salmon, Salmo salar L., post-smolts. Aquaculture 250:516–524

    Article  Google Scholar 

  • Fjelldal PG, Lock EJ, Grotmol S, Totland GK, Nordgarden U, Flik G, Hansen T (2006) Impact of smolt production strategy on vertebral growth and mineralisation during smoltification and the early seawater phase in Atlantic salmon (Salmo salar L.). Aquaculture 261:715–728

    Article  Google Scholar 

  • Fjelldal PG, Nordgarden U, Hansen T (2007a) The mineral content affects vertebral morphology in underyearling smolt of Atlantic salmon (Salmo salar L.). Aquaculture 270:231–239

    Article  CAS  Google Scholar 

  • Fjelldal PG, Hansen TJ, Berg AE (2007b) A radiological study on the development of vertebral deformities in cultured Atlantic salmon (Salmo salar L.). Aquaculture 273:721–728

    Article  Google Scholar 

  • Hansen T, Stefansson SO, Taranger GL (1992) Growth and sexual maturation in Atlantic salmon, Salmo salar L., reared in sea cages at two different light regimes. Aquacult Fish Manage 23:275–280

    Google Scholar 

  • Houde ED, Schekter RC (1981) Growth rate, rations and cohort consumption of marine fish larvae in relation to prey concentration. Rapp P-V Reun Cons Int Explor Mer 178:441–453

    Google Scholar 

  • Ince BW (1980) Amino acid stimulation of insulin secretion from the in situ perfused eel pancreas; modifications by somatostatin, adrenaline and theophylline. Gen Comp Endocrinol 40:275–282

    Article  PubMed  CAS  Google Scholar 

  • Maisse G, Noel O, Breton B, Goardon L, Le Bail PY, Mourot B (1998) Influence of a continuous light period on the first sexual maturation of the rainbow trout (Oncorhynchus mykiss). Bull Fr Peche Piscicult 350–351:255–264

    Article  Google Scholar 

  • Matty AJ (1986) Nutrition, hormones and growth. Fish Physiol Biochem 2:141–150

    Article  CAS  Google Scholar 

  • Millward DJ (1989) The nutritional regulation of muscle growth and protein turnover. Aquaculture 79:1–28

    Article  CAS  Google Scholar 

  • Murat J-C, Plisetskaya EM, Woo NYS (1981) Endocrine control of nutrition in cyclostomes and fish. Comp Biochem Physiol 68A:149–158

    Article  CAS  Google Scholar 

  • Nordgarden U, Oppedal F, Taranger GL, Hemre GI, Hansen T (2003) Seasonally changing metabolism in Atlantic salmon (Salmo salar L.) I—Growth and feed conversion ratio. Aquacult Nutr 9:287–293

    Article  CAS  Google Scholar 

  • Nordgarden U, Fjelldal PG, Hansen T, Björnsson BT, Wargelius A (2006) Growth hormone and insulin-like growth factor-I act together and independently when regulating growth in vertebral and muscle tissue of Atlantic salmon postsmolts. Gen Comp Endocrinol 149:253–260

    Article  PubMed  CAS  Google Scholar 

  • Oppedal F, Taranger GL, Hansen T (2003) Growth performance and sexual maturation in diploid and triploid Atlantic salmon (Salmo salar L.) in seawater tanks exposed to continuous light or simulated natural photoperiod. Aquaculture 215:145–162

    Article  Google Scholar 

  • Oppedal F, Berg A, Olsen RE, Taranger GL, Hansen T (2006) Photoperiod in seawater influence seasonal growth and chemical composition in autumn sea-transferred Atlantic salmon (Salmo salar L.) given two vaccines. Aquaculture 254:396–410

    Article  CAS  Google Scholar 

  • Plisetskaya EM, Buchelli-Narvaez LI, Hardy RW, Dickhoff WW (1991) Effects of injected and dietary arginine on plasma insulin levels and growth of pacific salmon and rainbow trout. Comp Biochem Physiol 98A:165–170

    Article  CAS  Google Scholar 

  • Rungruangsak K, Utne F (1981) Effect of different acidified wet feeds on protease activities in the digestive tract and on growth rate of rainbow trout (Salmo gairdneri Richardson). Aquaculture 22:67–79

    Article  CAS  Google Scholar 

  • Rungruangsak-Torrissen K (2007) Digestive efficiency, growth and qualities of muscle and oocyte in Atlantic salmon (Salmo salar L.) fed on diets with krill meal as an alternative protein source. J Food Biochem 31:509–540

    Article  CAS  Google Scholar 

  • Rungruangsak-Torrissen K, Fosseidengen JE (2007) Effect of artificial feeding on digestive efficiency, growth and qualities of muscle and oocyte of maturing Atlantic mackerel (Scomber scombrus L.). J Food Biochem 31:726–747

    Article  CAS  Google Scholar 

  • Rungruangsak Torrissen K, Male R (2000) Trypsin isozymes: development, digestion and structure. In: Haard NF, Simpson BK (eds) Seafood enzymes, utilization and influence on postharvest seafood quality. Marcel Dekker, New York, USA, pp 215–269

    Google Scholar 

  • Rungruangsak-Torrissen K, Stensholt BK (2001) Spatial distribution of Atlantic salmon post-smolts: association between genetic differences in trypsin isozymes and environmental variables. In: Kruse GH, Bez N, Booth A, Dorn MW, Hills S, Lipcius RN, Pelletier D, Roy C, Smith SJ, Witherell D (eds) Spatial processes and management of marine populations. University of Alaska Sea Grant, Fairbanks, USA, AK-SG-01–02, pp 415–429

    Google Scholar 

  • Rungruangsak-Torrissen K, Sundby A (2000) Protease activities, plasma free amino acids and insulin at different ages of Atlantic salmon (Salmo salar L.) with genetically different trypsin isozymes. Fish Physiol Biochem 22:337–347

    Article  CAS  Google Scholar 

  • Rungruangsak-Torrissen K, Carter CG, Sundby A, Berg A, Houlihan DF (1999a) Maintenance ration, protein synthesis capacity, plasma insulin and growth of Atlantic salmon (Salmo salar L.) with genetically different trypsin isozymes. Fish Physiol Biochem 21:223–233

    Article  CAS  Google Scholar 

  • Rungruangsak-Torrissen K, Wergeland HI, Glette J, Waagbø R (1999b) Disease resistance and immune parameters in Atlantic salmon (Salmo salar L.) with genetically different trypsin isozymes. Fish Shellfish Immunol 9:557–568

    Article  CAS  Google Scholar 

  • Rungruangsak-Torrissen K, Rustad A, Sunde J, Eiane SA, Jensen HB, Opstvedt J, Nygård E, Samuelsen TA, Mundheim H, Luzzana U, Venturini G (2002) In vitro digestibility based on fish crude enzyme extract for prediction of feed quality in growth trials. J Sci Food Agric 82:644–654

    Article  CAS  Google Scholar 

  • Rungruangsak-Torrissen K, Moss R, Andresen LH, Berg A, Waagbø R (2006) Different expressions of trypsin and chymotrypsin in relation to growth in Atlantic salmon (Salmo salar L.). Fish Physiol Biochem 32:7–23

    Article  CAS  Google Scholar 

  • Skrede A, Berge GM, Storebakken T, Herstad O, Aarstad KG, Sundstol F (1998) Digestibility of bacterial protein grown on natural gas in mink, pigs, chicken and Atlantic salmon. Anim Feed Sci Technol 76:103–116

    Article  CAS  Google Scholar 

  • Stryer L (1988) Biochemistry, 3rd edn. WH Freeman, New York, USA

    Google Scholar 

  • Sundby A, Eliassen K, Refstie T, Plisetskaya EM (1991) Plasma levels of insulin, glucagon and glucagon-like peptide in salmonids of different weights. Fish Physiol Biochem 9:223–230

    Article  CAS  Google Scholar 

  • Sunde J (2006) Digestive protease activities, growth and feed utilisation in Atlantic salmon (Salmo salar L.). Ph.D. thesis, Institute of Marine Research and University of Bergen, Norway, ISBN 82-308-0128-2

  • Sunde J, Taranger GL, Rungruangsak-Torrissen K (2001) Digestive protease activities and free amino acids in white muscle as indicators for feed conversion efficiency and growth rate in Atlantic salmon (Salmo salar L.). Fish Physiol Biochem 25:335–345

    Article  Google Scholar 

  • Sunde J, Eiane SA, Rustad A, Jensen HB, Opstvedt J, Nygård E, Venturini G, Rungruangsak-Torrissen K (2004) Effect of fish feed processing conditions on digestive protease activities, free amino acid pools, feed conversion efficiency and growth in Atlantic salmon (Salmo salar L.). Aquacult Nutr 10:261–277

    Article  CAS  Google Scholar 

  • Supannapong P, Pimsalee T, A-komol T, Engkagul A, Kovitvadhi U, Kovitvadhi S, Rungruangsak-Torrissen K (2008) Digestive enzymes and in-vitro digestability of different species of phytoplankton for culture of the freshwater pearl mussel, Hyriopsis (Hyriopsis) bialatus. Aquacult Int. doi:10.1007/s10499-007-9156-4

  • Taranger GL, Aardal L, Hansen T, Kjesbu OS (2006) Continuous light delays sexual maturation and increases growth in Atlantic cod (Gadus morhua L.) in sea cages. ICES J Mar Sci 63:365–375

    Article  Google Scholar 

  • Torrissen KR, Torrissen OJ (1984) Digestive proteases of Atlantic salmon (Salmo salar) from different river strains: development after hatching, rearing temperature effect and effect of sex and maturation. Comp Biochem Physiol 77B:15–20

    CAS  Google Scholar 

  • Torrissen KR, Lied E, Espe M (1994) Differences in digestion and absorption of dietary protein in Atlantic salmon (Salmo salar) with genetically different trypsin isozymes. J Fish Biol 45:1087–1104

    Article  CAS  Google Scholar 

  • Torrissen KR, Lied E, Espe M (1995) Differences in utilization of dietary proteins with varying degrees of partial pre-hydrolysis in Atlantic salmon (Salmo salar L.) with genetically different trypsin isozymes. In: Svasti J, Rimphanitchayakit V, Tassanakajorn A, Pongsawasdi P, Sonthayanon B, Packdibamrung K, Soontaros S, Limpaseni T, Wilairat P, Boonjawat J, Kamolsiripichaiporn S (eds) Biopolymers and bioproducts: structure, function and applications. Proceedings of the 11th FAOBMB Symposium (IUBMB Symposium No. 239), Samakkhisan (dokya) Public Company Limited, Bangkok, Thailand, pp 432–442

  • Unwin MJ, Rowe DK, Poortenaar CW, Boustead NC (2005) Suppression of maturation in 2-year-old Chinook salmon (Oncorhynchus tshawytscha) reared under continuous photoperiod. Aquaculture 246:239–250

    Article  Google Scholar 

  • Wargelius A, Fjelldal PG, Benedet S, Hansen T, Bjornsson BT, Nordgarden U (2005) A peak in gh-receptor expression is associated with growth activation in Atlantic salmon vertebrae, while upregulation of igf-I receptor expression is related to increased bone density. Gen Comp Endocrinol 142:163–168

    Article  PubMed  CAS  Google Scholar 

  • Waters (1993) Waters AccQ-Tag Chemistry Package Instruction Manual. Waters Corporation, Milford, MA, USA

  • Witten PE, Gil-Martens L, Hall BK, Huysseune A, Obach A (2005) Compressed vertebrae in Atlantic salmon Salmo salar: evidence for metaplastic chondrogenesis as a skeletogenic response late in ontogeny. Dis Aquat Org 64:237–246

    Article  PubMed  Google Scholar 

  • Wolnicki J, Myszkowski L, Korwin-Kossakowski M, Kaminski R, Andrzej Stanny L (2005) Effects of different diets on juvenile tench, Tinca tinca (L.) reared under controlled conditions. Aquacult Int 14:89–98

    Article  Google Scholar 

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  1. Jan Sunde

    Present address: Geno, 2326, Hamar, Norway

Authors and Affiliations

  1. Institute of Marine Research, Matre Research Station, 5984, Matredal, Norway

    Krisna Rungruangsak-Torrissen, Jan Sunde, Arne Erik Berg, Ulla Nordgarden, Per Gunnar Fjelldal & Frode Oppedal

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  1. Krisna Rungruangsak-Torrissen
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Correspondence to Krisna Rungruangsak-Torrissen.

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Rungruangsak-Torrissen, K., Sunde, J., Berg, A.E. et al. Digestive efficiency, free amino acid pools and quality of growth performance in Atlantic salmon (Salmo salar L.) affected by light regimes and vaccine types. Fish Physiol Biochem 35, 255–272 (2009). https://doi.org/10.1007/s10695-008-9206-5

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