Fish Physiology and Biochemistry

, Volume 41, Issue 6, pp 1369–1381 | Cite as

Effects on the metabolism, growth, digestive capacity and osmoregulation of juvenile of Sub-Antarctic Notothenioid fish Eleginops maclovinus acclimated at different salinities

  • L. Vargas-Chacoff
  • E. Saavedra
  • R. Oyarzún
  • E. Martínez-Montaño
  • J. P. Pontigo
  • A. Yáñez
  • I. Ruiz-Jarabo
  • J. M. Mancera
  • E. Ortiz
  • C. Bertrán


In this study we assessed the influence of three different environmental salinities (5, 15 and 31 psu during 90 days) on growth, osmoregulation, energy metabolism and digestive capacity in juveniles of the Notothenioid fish Eleginops maclovinus. At the end of experimental time samples of plasma, liver, gill, intestine, kidney, skeletal muscle, stomach and pyloric caeca were obtained. Growth, weight gain, hepatosomatic index and specific growth rate increased at 15 and 31 psu and were lower at 5 psu salinity. Gill Na+, K+-ATPase (NKA) activity presented a “U-shaped” relationship respect to salinity, with its minimum rates at 15 psu, while this activity correlated negatively with salinity at both anterior and posterior intestinal portions. No significant changes in NKA activity were observed in kidney or mid intestine. Large changes in plasma, metabolite levels and enzymatic activities related to energy metabolism in liver, gill, intestine, kidney and muscle were generally found in the groups exposed to 5 and 31 psu compared to the 15 psu group. Only the pepsin activity (digestive enzymes) assessed enhanced with environmental salinity, while pyloric caeca trypsin/chymotrypsin ratio decreased. This study suggests that juvenile of E. maclovinus presents greater growth near its iso-osmotic point (15 psu) and hyperosmotic environment (31 psu). Acclimation to low salinity increased the osmoregulatory expenditure as seen by the gill and anterior intestine results, while at high salinity, branchial osmoregulatory activity was also enhanced. This requires the mobilization of lipid stores and amino acids, thereby holding the growth of fish back. The subsequent reallocation of energy sources was not sufficient to maintain the growth rate of fish exposed to 5 psu. Thus, E. maclovinus juveniles present better growth efficiencies in salinities above the iso-osmotic point and hyperosmotic environment of this species, showing their best performance at 15 psu as seen by the main osmoregulatory and energy metabolism enzymatic activities.


Eleginops maclovinus Euryhaline fish Metabolism Growth Osmoregulation 



This study was carried out in the framework of FONDECYT Project 1110235 and FONDAP-INCAR, No. 15110027. We thank Dr. Lafayette Eaton and the Dirección de Investigación of the Universidad Austral de Chile (DID) for their help checking this manuscript.

Conflict of interest

The authors declare that there are no conflicts of interest.


  1. Alarcón FJ, Díaz M, Moyano FJ, Abellán E (1998) Characterization and functional properties of digestive proteases in two sparids; gilthead seabream (Sparus aurata) and common dentex (Dentex dentex). Fish Physiol Biochem 19:257–267CrossRefGoogle Scholar
  2. Appel W (1974) Leucine aminopeptidase determination with L-leucinamide as substrate. In: Bergmeyer HU (ed) Methods of Enzymatic Analysis. Academis Press, New York, pp 954–958CrossRefGoogle Scholar
  3. Applebaum SL, Peréz R, Lazo JP, Holt GJ (2001) Characterization of chymotrypsin activity during early ontogeny of larval red drum (Sciaenops ocellatus). Fish Physiol Biochem 25:291–300CrossRefGoogle Scholar
  4. Arjona FJ, Vargas-Chacoff L, Ruiz-Jarabo I, Martín del Río MP, Mancera JM (2007) Osmoregulatory response of Senegalase sole (Solea senegalensis, Kaup 1858) to changes in environmental salinity. Comp Biochem Physiol A 148:413–421CrossRefGoogle Scholar
  5. Arjona FJ, Vargas-Chacoff L, Ruiz-Jarabo I, Gonçalves O, Páscoa I, Martín del Río MP, Mancera JM (2009) Tertiary stress responses in Senegalese sole (Solea senegalensis Kaup, 1858) to osmotic acclimation: implications for osmoregulation, energy metabolism and growth. Aquaculture 287:419–426CrossRefGoogle Scholar
  6. Asha-Devi R, Aravindan AM (1997) Influence of salinity on the digestive enzyme activity of Oreochromis mossambicus (Peters). J Inland Fish Soc India 29:1–6Google Scholar
  7. Barman UK, Jana SN, Garg SK, Bhatnagar A, Arasu ART (2005) Effect of inland water salinity on growth, feed conversion efficiency and intestinal enzyme activity in growing grey mullet Mugil cephalus (Linn.): field and laboratory studies. Aquacult Int 13:241–256CrossRefGoogle Scholar
  8. Bath RN, Eddy FB (1979) Ionic and respiratory regulation in rainbow trout during rapid transfer to seawater. J Comp Physiol 134:351–357CrossRefGoogle Scholar
  9. Boeuf G, Payan P (2001) How should salinity influence fish growth? Comp Biochem Physiol C 130:411–423Google Scholar
  10. Bolasina S, Perez A, Yamashita Y (2006) Digestive enzyme activity during ontogenetic development and e¡ect of starvation in Japanese founder, Paralichthys olivaceus. Aquaculture 252:503–515CrossRefGoogle Scholar
  11. Erlanger B, Kokowsky N, Cohen W (1961) The preparation and properties of two new chromogenic substrates of trypsin. Arch Biochem Biophys 95:271–278CrossRefPubMedGoogle Scholar
  12. Gjellesvik DR, Lombardo D, Walther BT (1992) Pancreatic bile salt dependent lipase from cod (Gadus morhua): purification and properties. Biochim Biophys Acta 1124:123–134CrossRefPubMedGoogle Scholar
  13. Herrera M, Vargas-Chacoff L, Hachero I, Ruíz-Jarabo I, Rodiles A, Navas J, Mancera JM (2009) Osmoregulatory changes in wedge sole (Dicologoglossa cuneata, Moreau 1881) after acclimation to different environmental salinities. Aquac Res 40:762–771CrossRefGoogle Scholar
  14. Hummel BCW (1959) A modified spectrophotometric determination of chymotrypsin, trypsin and thrombin. Can J Biochem Physiol 37:1393–1399CrossRefPubMedGoogle Scholar
  15. Imsland AK, Foss A, Gunnarsson S, Berntssen MHG, FitzGerald R, Wendelaar Bonga S, Ham E, Naevdal G, Stefansson SO (2001) The interaction of temperature and salinity on growth and food conversion in juvenile turbot (Scophthalmus maximus). Aquaculture 198:353–367CrossRefGoogle Scholar
  16. Jensen MK, Madsen SS, Kristiansen K (1998) Osmoregulation and salinity effects on the expression and activity of Na+-K+ ATPase in the gills of European sea bass, Dicentrarchus labrax (L.). J Exp Zool 282:290–300CrossRefPubMedGoogle Scholar
  17. Keppler D, Decker K (1974) Glycogen. Determination with amyloglucosidase. In: Bergmeyer HU (ed) Methods of enzymatic analysis. Academic, New York, pp 1127–1131Google Scholar
  18. Kirschner LB (1995) Energetics of osmoregulation in fresh water vertebrates. J Exp Zool 271:243–252CrossRefGoogle Scholar
  19. Laiz-Carrión R, Sangiao-Alvarellos S, Guzmán JM, Martín del Río MP, Soengas JL, Mancera JM (2005) Growth performance on gilthead sea bream Sparus aurata in different osmotic conditions: implications on osmoregulation and energy metabolism. Aquaculture 250:849–861CrossRefGoogle Scholar
  20. Mancera JM, McCormick SD (2007) Role of prolactin, growth hormone, insuline-like growth factor and cortisol in teleost osmoregulation. In: Baldisserotto B, Mancera JM, Kapoor BG (eds) Fish Osmoregulation. Science Publishers, New York, pp 497–515CrossRefGoogle Scholar
  21. Mancera JM, Laiz-Carrión R, Martín del Río MP (2002) Osmoregulatoryaction of PRL, GH, and cortisol in the gilthead seabream (Sparus aurata L.). Gen Comp Endocrinol 129:95–103CrossRefGoogle Scholar
  22. Marshall WS (2002) Na+, Cl, Ca++ and Zn++ transport by fish gills: retrospective review and prospective synthesis. J Exp Zool 292:264–283CrossRefGoogle Scholar
  23. McCormick SD (1993) Methods for nonlethal gill biopsy and measurement of Na+-K+ ATPase activity. Can J Fish Aquat Sci 50:656–658CrossRefGoogle Scholar
  24. McCormick SD (1995) Hormonal control of gill Na+, K+-ATPase and chloride cell function. In: Wood CM, Shuttlewoth TJ (eds) Fish Physiology, vol XIV., Ionoregulation: cellular and molecular approachesAcademic Press, New York, pp 285–315Google Scholar
  25. Moore S (1968) Amino acid analysis: aqueous dimethyl sulfoxide as solvent for the ninhydrin reaction. J Chem Biol 1242:6281–6283Google Scholar
  26. Moutou KA, Panagiotaki P, Mamuris Z (2004) Effects of salinity on digestive protease activity in the euryhaline sparid Sparus aurata L.: a preliminary study. Aquacult Int 35:912–914Google Scholar
  27. Nikolopoulou D, Moutou KA, Fountoulaki E, Venou B, Adamidou S, Alexis MN (2011) Patterns of gastric evacuation, digesta characteristics and pH changes along the gastrointestinal tract of gilthead sea bream (Sparus aurata L.) and European sea bass (Dicentrarchus labrax L.). Comp Biochem Physiol A 158:406–414CrossRefGoogle Scholar
  28. Pequeño G, Pavés H, Bertrán C, Vargas-Chacoff L (2010) Seasonal limnetic feeding regime of the “robalo” Eleginops maclovinus (Valenciennes 1830), in the Valdivia river, Chile. Gayana 74:47–56Google Scholar
  29. Psochiou E, Mamuris Z, Panagiotaki P, Kouretas D, Mountou KA (2007) The response of digestive proteases to abrupt salinity decrease in the euryhaline sparid Sparus aurata L. Comp Biochem Physiol B 147:156–163CrossRefPubMedGoogle Scholar
  30. Quinn GP, Keough MJ (2002) Experimental design and data analysis for biologists. Cambridge University Press, United KingdomCrossRefGoogle Scholar
  31. Rungruangsak-Torrisen 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 31:509–540CrossRefGoogle Scholar
  32. Rungruangsak-Torrisen K, Moss R, Andresen LH, Berg A, Waagbø R (2006) Different expressions of trypsin and chimotrypsin in relation to growth in salmon (Salmo salar). Fish Physiol Biochem 32:7–23CrossRefGoogle Scholar
  33. Sá R, Gavilán M, Rioseco MJ, Llancabure A, Vargas-Chacoff L, Augsburger A, Bas F (2014) Dietary protein requirement of Patagonian blennie (Eleginops maclovinus, Cuvier 1830) juveniles. Aquaculture 428–429:125–134CrossRefGoogle Scholar
  34. Salas-Leitón EA, Rodriguez-Rúa A, Asensio E, Infante C, Manchado M, Fernández-Díaz C, Cañavate JP (2012) Effect of salinity on egg hatching, yolk sac absorption and larval rearing of Senegalese sole (Solea senegalensis Kaup 1858). Rev Aquacult 4:49–58CrossRefGoogle Scholar
  35. Sangiao-Alvarellos S, Laiz-Carrión R, Guzmán JM, Martín del Río MP, Mancera JM, Soengas JL (2003) Acclimation of Sparus aurata to various salinities alters energy metabolism of osmoregulatory and and nonosmoregulatory organs. Am J Physiol 285:897–907Google Scholar
  36. Sangiao-Alvarellos S, Arjona FJ, Martín del Río MP, Míguez MP, Mancera JM, Soengas JL (2005) Time course of osmoregulatory and metabolic changes during osmotic acclimation in Sparus auratus. J Exp Biol 208:4291–4304CrossRefPubMedGoogle Scholar
  37. Sarath G, De la Monte RS, Warner FW (1989) Protease assay methods. In: Beyon RJ, Bond JS (eds) Proteolytic enzymes: a practical approach. Oxford University Press, New York, pp 25–56Google Scholar
  38. Soengas JL, Sangiao-Alvarellos S, Laiz-Carrión R, Mancera JM (2007) Energy metabolism and osmotic acclimation in teleost fish. In: Baldisserotto B, Mancera JM, Kapoor BG (eds) Fish osmoregulation. Science Publishers, Enfield, pp 277–308CrossRefGoogle Scholar
  39. Taylor JR, Grosell M (2006) Feeding and osmoregulation: dual function of the marine teleost intestine. J Exp Biol 209:2939–2951CrossRefPubMedGoogle Scholar
  40. Tipsmark CK, Madsen SS, Seidelin M, Christensen AS, Cutler CP, Cramb G (2002) Dynamics of Na+, K+, 2Cl cotransporter and Na+, K+-ATPase expression in the branchial epithelium of brown trout (Salmo trutta) and Atlantic salmon (Salmo salar). J Exp Zool 293:106–118CrossRefPubMedGoogle Scholar
  41. Tsuzuki MY, Sugai JK, Maciel JC, Francisco CJ, Cerqueira VR (2007) Survival, growth and digestive enzyme activity of juveniles of the fat snook (Centropomus parallelus) reared at different salinities. Aquaculture 271:319–325CrossRefGoogle Scholar
  42. Vargas-Chacoff L, Arjona FJ, Polakof S, Martín del Río MP, Soengas JL, Mancera JM (2009a) Interactive effects of environmental salinity and temperature on metabolic responses of gilthead sea bream Sparus aurata. Comp Biochem Physiol A 154:417–424CrossRefGoogle Scholar
  43. Vargas-Chacoff L, Arjona FJ, Ruiz-Jarabo I, Páscoa I, Gonçalves O, Martín del Río MP, Mancera JM (2009b) Seasonal variation in osmoregulatory and metabolic parameters in earthen pond cultured gilthead sea bream Sparus aurata. Aquac Res 40:1279–1290CrossRefGoogle Scholar
  44. Vargas-Chacoff L, Calvo A, Ruiz-Jarabo I, Villarroel F, Muñoz JL, Tinoco AB, Cárdenas S, Mancera JM (2011) Growth performance, osmoregulatory and metabolic modifications in red porgy fry, Pagrus pagrus, under different environmental salinities and stocking densities. Aquac Res 42:1269–1278CrossRefGoogle Scholar
  45. Vargas-Chacoff L, Moneva F, Oyarzún R, Martínez D, Muñóz JLP, Bertrán C, Mancera JM (2014a) Environmental salinity-modified osmoregulatory response in the Sub-Antarctic notothenioid fish Eleginops maclovinus. Polar Biol 37:1235–1245CrossRefGoogle Scholar
  46. Vargas-Chacoff L, Ortíz E, Oyarzún R, Martínez D, Saavedra E, Sá R, Olavarría V, Yáñez A, Bertrán C, Mancera JM (2014b) Stocking density and Piscirickettsia salmonis infection affect the skeletal muscle intermediate metabolism in Eleginops maclovinus. Fish Physiol Biochem 40:1683–1691CrossRefPubMedGoogle Scholar
  47. Vargas-Chacoff L, Martínez D, Oyarzún R, Nualart D, Olavarría V, Yáñez A, Bertrán C, Ruiz-Jarabo I, Mancera JM (2014c) Combined effects of high stocking density and Piscirickettsia salmonis treatment on the immune system, metabolism and osmoregulatory responses of the Sub-Antarctic Notothenioid fish Eleginops maclovinus. Fish Shellfish Immun 40:424–434CrossRefGoogle Scholar
  48. Vijayan MM, Foster GD, Moon TW (1993) Effects of cortisol on hepatic carbohydrate metabolism and responsiveness to hormones in the sea raven Hemitripterus americanus. Fish Physiol Biochem 12:327–335CrossRefPubMedGoogle Scholar
  49. Vijayan MM, Reddy PK, Leatherland JF, Moon TW (1994) The effects of cortisol on hepatocyte metabolism in rainbow trout: a study using the steroid analogue RU486. Gen Comp Endocrinol 96:75–84CrossRefPubMedGoogle Scholar
  50. Walter HE (1984) Proteinases: methods with hemoglobin, casein and azocoll as substrates. In: Bergmeyer HJ (ed) Methods of enzymatic analysis, vol V. Verlag Chemie, Weinham, pp 270–277Google Scholar
  51. Wendelaar-Bonga SE (1997) The stress response in fish. Physiol Rev 77:591–625PubMedGoogle Scholar
  52. Worthington K, Worthington V (2011) Worthington Biochemical Corporation date of access. Worthington Enzime Manual. (
  53. Zambonino-Infante JL, Cahu CL (2001) Ontogeny of the gastrointestinal tract of marine fish larvae. Comp Biochem Physiol C 130:477–487Google Scholar

Copyright information

© Springer Science+Business Media Dordrecht 2015

Authors and Affiliations

  • L. Vargas-Chacoff
    • 1
  • E. Saavedra
    • 1
  • R. Oyarzún
    • 1
  • E. Martínez-Montaño
    • 2
    • 3
  • J. P. Pontigo
    • 1
    • 4
  • A. Yáñez
    • 4
  • I. Ruiz-Jarabo
    • 5
    • 6
  • J. M. Mancera
    • 5
  • E. Ortiz
    • 1
  • C. Bertrán
    • 1
  1. 1.Instituto de Ciencias Marinas y LimnológicasUniversidad Austral de ChileValdiviaChile
  2. 2.Centro de Investigación y Desarrollo (CIEN Austral) CONICYT Regional R10C1002Universidad Austral de ChilePuerto MonttChile
  3. 3.Facultad de Ciencias del MarUniversidad Autónoma de SinaloaMazatlánMexico
  4. 4.Instituto de Bioquímica y Microbiología, Interdisciplinary Center for Aquaculture Research (FONDAP-INCAR)Universidad Austral de ChileValdiviaChile
  5. 5.Departamento de Biología, Facultad de Ciencias del Mar y Ambientales, Campus de Excelencia Internacional del Mar (CEI-MAR)Universidad de CádizCádizSpain
  6. 6.Centre of Marine Sciences (CCMar), CIMAR-Laboratório AssociadoUniversidade do AlgarveFaroPortugal

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