Advertisement

Fish Physiology and Biochemistry

, Volume 45, Issue 1, pp 469–484 | Cite as

Lipid digestion capacity in gilthead seabream (Sparus aurata) from first feeding to commercial size

  • Leire ArantzamendiEmail author
  • Francisco Roo
  • Carmen María Hernández-Cruz
  • Hipólito Fernández-Palacios
  • Marisol Izquierdo
Article

Abstract

To characterise the progression of lipid digestion capacity in gilthead seabream across life cycle, the activities of bile salt-activated lipase (BAL) and phospholipase A2 (PLA2) were determined in the digestive tracts of cultured gilthead seabream from first feeding to marketable size (49 μg to 300 g). Four trials were undertaken with gilthead seabream of different ages, fed on diets with fishmeal and fish oil as the main dietary protein and lipid sources and 21–25% lipid contents. Larvae of 4 days after hatching (dah) to 9 dah were fed rotifers with different fatty acid profiles: control (2.8% eicosapentaenoic acid, EPA; 1.6% docosahexaenoic acid, DHA; 5.4% n-3 long-chain polyunsaturated fatty acids, n-3 LC-PUFAs; and 0.2% arachidonic acid, ARA), low EPA (1.38% EPA, 1.6% DHA, 3.9% n-3 LC-PUFA and 0.4% ARA) or low LC-PUFA (0.7% EPA, 1.0% DHA, 1.8% n-3 LC-PUFA and 0.0% ARA) (% dry weight). Larvae fed the low-LC-PUFA diet showed a significantly lower growth at 10 dah. BAL activities were significantly higher in larvae fed the control diet than in those fed low-EPA and low-LC-PUFA diets at 9 dah. BAL activity increased with age across life cycle (49 μg to 300 g). PLA2 activity could not be detected in larvae but increased with age in juvenile and adult gilthead seabream (86 g to 295 g), similar to BAL. Results suggested a correspondence between the stimulation of lipid digestion capacity and growth performance in gilthead seabream by dietary essential fatty acids, particularly by EPA when DHA requirements are met in the diet especially in the very early stages of life cycle, when the progression of BAL and PLA2 activities could be used as indicators of the nutritional status of cultured gilthead seabream larvae. Finally, regarded that PLA2 activity was not detected in 4-dah to 44-dah gilthead seabream larvae, future works are suggested to assess the dietary effect on PLA2 activity and the PLA2 activity pattern along the larval stage of this species using a more sensitive detection method.

Keywords

Seabream Digestive capacity Bile salt-activated lipase Phospholipase A2 EPA DHA 

Notes

Acknowledgments

The authors of the present work would like to acknowledge all members of GIA (Grupo de Investigación en Acuicultura) IU-Ecoaqua from ULPGC for their technical support and provision and management of gilthead seabream broodstock and spawning.

Author’s contributions

Marisol Izquierdo conceived of and designed the experiments. Leire Arantzamendi analysed the experimental results and wrote the paper. Javier Roo conducted the rotifer culture and their enrichment with lipid emulsions and baker’s yeast. Carmen Maria Hernández-Cruz and Leire Arantzamendi conducted the larval rearing and measurements of growth parameters. Leire Arantzamendi conducted the dissection of larvae and, together with Marisol Izquierdo, conducted the enzymatic assays. Hipólito Fernández-Palacios conducted the management of broodstock and the spawning. Leire Arantzamendi conducted the rearing of juvenile and adult gilthead seabream. This paper is contribution nº 883 from AZTI (Marine research).

Compliance with ethical standards

All applicable international, national, and/or institutional guidelines for the care and use of animals were followed.

Conflict of interest

The authors declare that they have no competing interests.

References

  1. Austreng E, Skrede A, Eldegard Å (1979) Effect of dietary fat source on the digestibility of fat and fatty acids in rainbow trout and mink. Acta Agric Scand 29:119–126CrossRefGoogle Scholar
  2. Benedito-Palos L, Ballester-Lozano G, Pérez-Sánchez J (2014) Wide-gene expression analysis of lipid-relevant genes in nutritionally challenged gilthead sea bream (Sparus aurata). Gene 547:34–42CrossRefGoogle Scholar
  3. Bessonart M, Izquierdo MS, Salhi M, Hernández-Cruz CM, González MM, Fernández-Palacios H (1999) Effect of dietary arachidonic acid levels on growth and survival of gilthead seabream (Sparus aurata L.) larvae. Aquaculture 179(1–4):265–275CrossRefGoogle Scholar
  4. Buchet V, Zambonino Infante JL, Cahu CL (2000) Effect of lipid level in a compound diet on the development of red drum (Sciaenops ocellatus) larvae. Aquaculture 184:339–347CrossRefGoogle Scholar
  5. Calzada A (1996) Desarrollo postembrionario del intestino y órganos asociados de la dorada, Sparus aurata L., en cultivo. Estudio histológico y ultraestructural. Ph D Thesis. University of Cádiz, SpainGoogle Scholar
  6. Calzada A, Medina A, González de Canales ML (1998) Fine structure of the intestine development in cultured seabream larvae. J Fish Biol 53:340–365CrossRefGoogle Scholar
  7. Christie WW (1989) Gas chromatography and lipids: a practical guide. The Oily Press, Ayr, pp 67–69Google Scholar
  8. Cousin JCB, Bauding-Laurencing F, Gabaudan J (1987) Ontogeny of enzimatic activities in fed and fasting turbot, Scophthalmus maximus L. J Fish Biol 30:15–33CrossRefGoogle Scholar
  9. Darias MJ, Murray HM, Gallant JW, Douglas SE, Yúfera M, Martínez-Rodríguez G (2007) The spatiotemporal expression pattern of trypsinogen and bile salt-activated lipase during the larval development of red porgy (Pagrus pagrus, Pisces, Sparidae). Mar Biol 152:109–118CrossRefGoogle Scholar
  10. Díaz JP, Connes R (1997) Ontogenesis of the biliary tract in a teleost, the sea bass Dicentrarchus labrax L. Canadian Journal of Zoology-Revue Can d Zool 75:740–745CrossRefGoogle Scholar
  11. Díaz JP, Guyot E, Vigier S, Connes R (1997a) First events in lipid absorption during post-embryonic development of the anterior intestine in gilt-head sea bream. J Fish Biol 51:180–192CrossRefGoogle Scholar
  12. Díaz JP, Mani-Ponset L, Guyot E, Connes R (1997b) Biliary lipid secretion during early post-embryonic development in three fishes of aquacultural interest: sea bass, Dicentrarchus labrax L, sea bream, Sparus aurata L, and pike-perch, Stizostedion lucioperca (L). J Exp Zool 277:365–370CrossRefGoogle Scholar
  13. Folch JM, Lees M, Stanley Sloane GH (1957) A simple method for the isolation and purification of total lipids from the animal tissues. J Biol Chem 226:497–509Google Scholar
  14. Fox C (1990) Studies on polyunsaturated fatty acid nutrition in larvae of marine fish- the herring, Clupea harengus L. Ph D Thesis, University of Stirling, Scotland, 196ppGoogle Scholar
  15. Gawlicka A, Parent B, Horn MH, Ross N, Opstad I, Torrissen OJ (2000) Activity of digestive enzymes in yolk-sac larvae of Atlantic halibut (Hippoglossus hippoglossus): indication of readiness for first feeding. Aquaculture 184:303–314CrossRefGoogle Scholar
  16. Guerrera MC, De Pascuale F, Muglia U, Caruso G (2015) Digestive enzymatic activity during ontogenetic development in zebrafish (Danio derio). J Exp Zool 324B:699–706CrossRefGoogle Scholar
  17. Hoehne-Reitan K, Kjørsvik E, Gjellesvik DR (2001a) Development of bile salt-dependent lipase and larval turbot. J Fish Biol 58:737–745CrossRefGoogle Scholar
  18. Hoehne-Reitan K, Kjørsvik E, Reitan I (2001b) Bile salt-dependent lipase in larval turbot, as influenced by density and lipid content of fed prey. J Fish Biol 58:746–754CrossRefGoogle Scholar
  19. Huang C, Zhou L, Liu Y, Lai (2006) A continuous fluerescence assay for phospholipase A2 with nontagged lipid. Analytical Biochemistry 351:11–17Google Scholar
  20. Iijima N, Nakamura M, Uematsu K, Kayama M (1990) Partial purification and characterization of phospholipase A2 from the hepatopancreas of red seabream Pagrus major. Nippon Suisan Gakkaishi 56:1331–1339CrossRefGoogle Scholar
  21. Iijima N, Chosa S, Uematsu K, Goto K, Toshiba T, Kayama M (1997) Purification and characterization of phospholipase A2 from the piloric caeca of red seabream, Pagrus major. Fish Physiol Biochem 16:487–498CrossRefGoogle Scholar
  22. Iijima N, Tanaka S, Ota Y (1998) Purification and characterization of bile salt-activated lipase from the hepatopancreas of red seabream, Pagrus major. Fish Physiol Biochem 18:59–69CrossRefGoogle Scholar
  23. Izquierdo MS, Henderson RJ (1998) The determination of lipase and phospholipase activities in gut contents of turbot (Scophthalmus maximus) by fluorescence-based assays. Fish Physiol Biochem 19:153–162CrossRefGoogle Scholar
  24. Izquierdo MS, Koven W (2011) Lipids. In: Holt J (ed) Larval fish nutrition. Wiley-Blackwell, John Wiley and Sons, Chichester, pp 47–84CrossRefGoogle Scholar
  25. Izquierdo MS, Watanabe T, Takeuchi T, Arakawa T, Kitajima C (1990) Optimum EFA levels in Artemia to meet the EFA requirements of red seabream (Pagrus major). In: Takeda M, Watanabe T (eds) The current status of fish nutrition in aquaculture. Tokyo University of Fisheries, Tokyo, pp 221–232Google Scholar
  26. Izquierdo MS, Socorro J, Arantzamendi L, Hernández-Cruz CM, Valencia A (2000) Recent advances in lipid nutrition in marine fish larvae. Fish Physiol Biochem 22:96–107CrossRefGoogle Scholar
  27. Izquierdo MS, Tandler A, Salhi M, Kolkovsky S (2001) Influence of dietary polar lipids’ quantity and quality on ingestion and assimilation of labelled fatty acids in larval gilthead seabream. Aquac Nutr 6:153–160CrossRefGoogle Scholar
  28. Kanazawa A (1985) Essential fatty acid and lipid requirement of fish. In: Cowey CB, Mackie AM, Bell JG (eds) Nutrition and feeding in fish. Academic, London, pp 287–298Google Scholar
  29. Kanazawa A, Koshio S, Teshima S (1989) Growth and survival of larval red seabream (Pagrus major) and Japanese flounder (Paralichthys olivaceous) fed microbound diets. J World Aquacult Soc 20:31–37CrossRefGoogle Scholar
  30. Kjørsvik E, Van der Meeren T, Kryvi H, Arnfinnson J, Kvenseth PG (1991) Early development of the digestive tract of cod larvae, Gadus morhua L., during start-feeding and starvation. J Fish Biol 38:1–15CrossRefGoogle Scholar
  31. Kolkovski S, Tandler A, GWm K, Gertler A (1993) The effect of dietary exogenous digestive enzymes on ingestion, assimilation, growth and survival of gilthead seabream larvae. Fish Physiol Biochem 12:203–209CrossRefGoogle Scholar
  32. Koven WM, Tandler A, Sklan D, Kissil GW (1993) The association of eicosapentaenoic and docosahexaenoic acids in the main phospholipids of different-age Sparus aurata larvae with growth. Aquaculture 116:71–82CrossRefGoogle Scholar
  33. Koven WM, Henderson RJ, Sargent JR (1994) Lipid digestion in turbot (Scopthalmus maximus) II: lipolysis in vitro of 14C-labeled triacylglycerol, cholesterol ester and phosphatidylcholine by digesta from different segments of the digestive tract. Fish Physiol Biochem 13:275–283CrossRefGoogle Scholar
  34. Koven WM, Henderson RJ, Sargent JR (1997) Lipid digestion in turbot (Scophthalmus maximus): in-vivo and in-vitro studies of the lipolytic activity in various segments of the digestive tract. Aquaculture 151:155–171CrossRefGoogle Scholar
  35. Koven W, Barr Y, Lutzky S, Ben-Atia I, Weiss R, Harel M, Behrens P, Tandler A (2001) The effect of dietary arachidonic acid (20: 4n-6) on growth, survival and resistance to handling stress in gilthead seabream (Sparus aurata) larvae. Aquaculture 193(1–2):107–122Google Scholar
  36. Lie O, Lied E, Lambertsen G (1987) Lipid digestion in cod (Gadus morhua). Comp Biochem Physiol B Comp Biochem 88(2):697–700CrossRefGoogle Scholar
  37. Liu J, Caballero MJ, El-Sayed Ali T, Izquierdo MS, Hernández Cruz CM, Valencia A, Fernández-Palacios H (2002) Necessity of dietary lecithin and eicosapentaenoic acid for growth, survival, stress resistance and lipoprotein formation in gilthead seabream (Sparus aurata). Fish Sci 68:1165–1172CrossRefGoogle Scholar
  38. Mansbach (2001) Triacylglicerol Movement in Enterocytes In: Mansbach CM II, Tso P, Kuksis A (eds) Intestinal lipid metabolism. Kluwer Academic/Plenum, New York pp 215–233Google Scholar
  39. Mata-Sotres JA, Martos-Sitcha JA, Astola A, Yúfera M, Martínez-Rodríguez G (2016a) Cloning and molecular ontogeny of digestive enzymes in fed and food-deprived developing gilthead seabream (Sparus aurata) larvae. Comp Biochem Physiol B 191:53–65CrossRefGoogle Scholar
  40. Mata-Sotres JA, Moyano FJ, Martínez-Rodríguez G, Yúfera M (2016b) Daily rhythms of digestive enzyme activity and gene expression in gilthead seabream (Sparus aurata) during ontogeny. Comp Biochem Physiol A 197:43–51CrossRefGoogle Scholar
  41. Morais S, Rojas-Garcia CR, Conceição LEC, Rønnestad I (2005) Digestion and absorption of a pure triacylglycerol and a free fatty acid by Clupea harengus L. larvae. J Fish Biol 67:223–238CrossRefGoogle Scholar
  42. Moyano FJ, Díaz M, Alarcon FJ, Sarasquete MC (1996) Characterization of digestive enzyme activity during larval development of gilthead seabream (Sparus aurata). Fish Physiol Biochem 15:121–130CrossRefGoogle Scholar
  43. Mukhopadhyay PK, Rout SK (1996) Effects of different dietary lipids on growth and tissue fatty acid changes in fry of the carp Catla catla (Hamilton). Aquac Res 27:623–630CrossRefGoogle Scholar
  44. Murashita K, Matsunari H, Kumon K, Tanaka Y, Shiozawa S, Furuita H, Oku H, Yamamoto T (2014) Characterization and ontogenetic development of digestive enzymes in Pacific bluefin tuna Thunnus orientalis larvae. Fish Physiol Biochem 40:1741–1755CrossRefGoogle Scholar
  45. Murray HM, Gallant JW, Perez-Casanova JC, Johnson SC, Douglas SE (2003) Ontogeny of lipase expression in winter flounder. J Fish Biol 62:816–833CrossRefGoogle Scholar
  46. Muzaffar Bazaz M, Keshavanath P (1993) Effect of feeding different levels of sardine oil on growth, muscle composition and digestive enzyme activities of masheer, Tor khudree. Aquaculture 115:111–119CrossRefGoogle Scholar
  47. Olsen RE, Henderson RJ, Ringo E (1998) The digestion and selective absorption of dietary fatty acids in Atlantic charr, Salvelinus alpinus. Aquac Nutr 4:13–21CrossRefGoogle Scholar
  48. Ono H, Iijima N (1998) Purification and characterization of phospholipase A2 from the hepatopancreas of red seabream, Pagrus major. Fish Physiol Biochem 18:135–147CrossRefGoogle Scholar
  49. Oozeki Y, Bailey KM (1995) Ontogenic development of digestive enzyme activities in larval walleye pollok, Theragra chalcogramma. Mar Biol 122:177–186Google Scholar
  50. Perez-Casanova JC, Murray HM, Gallant JW, Ross NW, Douglas SE, Johnson SC (2006) Development of the digestive capacity in larvae of haddock (Melanogrammus aeglefinus) and Atlantic cod (Gadus morhua). Aquaculture 251:377–401CrossRefGoogle Scholar
  51. Ribeiro L, Sarasquete C, Dinis MT (1999) Histological and histochemical development of the digestive system of Solea senegalensis (Kaup, 1858) larvae. Aquaculture 171:293–308CrossRefGoogle Scholar
  52. Rodríguez C, Pérez JA, Díaz M, Izquierdo MS, Hernández-Palacios H, Lorenzo A (1997) Influence of the EPA/DHA ratio in rotifers on gilthead seabream (Sparus aurata) larval development. Aquaculture 150:77–89CrossRefGoogle Scholar
  53. Rønnestad I, Finn RN, Lein I, Lie O (1995) Compartamental changes in the contents of total lipid, lipid classes and their associated fatty acids in the developing yolk-sac larvae of Atlantic halibut Hippoglossus hippoglossus (L.). Aquac Res 1:119–130Google Scholar
  54. Rønnestad I, Yúfera M, Ueberschär B, Ribeiro L, Sæle Ø, Boglione C (2013) Feeding behaviour and digestive physiology in larval fish: current knowledge, and gaps and bottlenecks in research. Rev Aquac 5(Suppl. 1):S59–S98CrossRefGoogle Scholar
  55. Rotllan G, Moyano FJ, Andrés M, Díaz M, Estévez A, Gisbert E (2008) Evaluation of fluorometric substrates in he assessment of digestive enzymes in a decapod Maja brachydactyla larvae. Aquaculture 282:90–96CrossRefGoogle Scholar
  56. Rudd EA, Brockman HL (1984) Pancreatic carboxyl ester lipase. In: Borgstrom M, Brockman HL (eds) Lipases. Elsevier, Amsterdam, pp 185–204Google Scholar
  57. Sæle Ø, Nordgreen A, Olsvik PA, Hamre K (2010) Characterization and expression of digestive neutral lipases during ontogeny of Atlantic cod (Gadus morhua). Comp Biochem Physiol A Mol Integr Physiol 157:252–259CrossRefGoogle Scholar
  58. Sæle Ø, Nordgreen A, Olsvik PA, Hamre K (2011) Characterisation and expression of secretory phospholipase A2 group IB during ontogeny of Atlantic cod (Gadus morhua). Br J Nutr 105:228–237CrossRefGoogle Scholar
  59. Saleh R, Betancor MB, Roo J, Benítez-Santana T, Hernández-Cruz CM, Moyano FJ, Izquierdo MS (2012) Optimum krill phospholipids contents in microdiets for gilthead seabream (Sparus aurata) larvae. Aquac Nutr.  https://doi.org/10.1111/j.1365-2095
  60. Saleh R, Betancor MB, Roo J, Benítez-Santana T, Hernández-Cruz CM, Moyano FJ, Izquierdo MS (2012) Optimum krill phospholipids contents in microdiets for gilthead seabream (Sparus aurata) larvae. Aquac Nutr. 19:449–460.  https://doi.org/10.1111/anu.12009
  61. Salhi M, Izquierdo MS, Hernández Cruz CM, González M, Fernández-Palacios H (1994) Effect of lipid and n-3 LC-PUFA levels in microdiets on growth, survival and fatty acid composition of larval gilthead seabream (Sparus aurata). Aquaculture 124(1–4):275–282CrossRefGoogle Scholar
  62. Sarasquete MC, Polo A, González de Canales ML (1993) A histochemical and inmunohistochemical study of digestive enzymes and hormones during the larval development of the seabream, Sparus aurata L. Histochem J 25:430–437CrossRefGoogle Scholar
  63. Slotboom A, Verheij HM, de Haas GH (1982) On the mechanism of phospholipase A2. In: Hawthorne JN, Ansell GB (eds) New York comprehensive biochemistry. Vol. 4, phospholipids. Elsevier Biomedical, Amsterdam, pp 359–434Google Scholar
  64. Srichanun M, Tantikitti C, Utarabhand P, Kortner T (2013) Gene expression and activity of digestive enzymes during the larval development of Assian seabass (Lates calcarifer). Comp Biochem Physiol B 165:1–9CrossRefGoogle Scholar
  65. Takeuchi T, Toyota M, Satoh S, Watanabe T (1990) Requirement of juvenile red sea bream Pagrus major for eicosapentaenoic and docosahexaenoic acids. Nippon Suisan Gakkaishi 56:1263–1269CrossRefGoogle Scholar
  66. Teshima S, Kanazawa A, Sakamoto S (1982) Microparticulate diets for the larvae of aquatic animals. Min Rev Data File Fish Res 2:67–86Google Scholar
  67. Toyota M, Takeuchi T, Watanabe T (1991) Dietary value to larval yellowtail of Artemia nauplii enriched with EPA and DHA. Abstracts of the annual meeting of the Japanese Society of Scientific Fisheries. April. TokyoGoogle Scholar
  68. Vallés R, Estévez A (2015) Effect of different enrichment products rich in docosahexaenoic acid on growth and survival of meagre, Argyrosomus regius (Asso, 1801). J World Aquacult Soc 46(2):191–200CrossRefGoogle Scholar
  69. Van den Bosch H (1980) Intracellular phospholipases A. Biochim Biophys Acta 604:191–246Google Scholar
  70. Van den Bosch H (1982) Phospholipases. In: Hawthorne JN, Ansell GB (eds) New comprehensive biochemistry. Phospholipids, vol 4. Elsevier Biochemical, Amsterdam, pp 313–357Google Scholar
  71. Verger R (1984) Pancreatic lipase. In: Borgstrom B, Brockman HL (eds) Lipase. Elsevier, Amsterdam, pp 83–15Google Scholar
  72. Waite M (1987) Pancreatic and snake venom phospholipase A2. In: Handbook of lipid research. Vol. 5. The phospholipases. Prenum, New York, pp 155–241Google Scholar
  73. Wang CS, Hartsuck JA (1993) Bile salt activated lipase. A multiple function lipolytic enzyme. Biochim Biophys Acta 1166:1–19CrossRefGoogle Scholar
  74. Watanabe T (1993) Importance of docosahexaenoic acid in marine larval fish. J World Aquacult Soc 24:152–161CrossRefGoogle Scholar
  75. Watanabe T, Izquierdo MS, Takeuchi T, Satoh S, Kitajima C (1989) Comparison between eicosapentaenoic and docosahexaenoic acids in terms of essential fatty acid efficacy in larval seabream. Nippon Suisan Gakkaishi 55:1635–1640CrossRefGoogle Scholar
  76. Wold PA, Hoehne-Reitan K, Cahu CL, Zambonino Infante JL, Rainuzzo J, Kjørsvik E (2007) Phospholipids vs. neutral lipids: effects on digestive enzymes in Atlantic cod (Gadus morhua) larvae. Aquaculture 272:502–513CrossRefGoogle Scholar
  77. Wu FC, Ting YY, Chen HY (2002) Docosahexaenoic acid is superior to eicosapentaenoic acid as the essential fatty acid for growth of grouper, Epinephelus malabaricus. J Nutr 132:72–79CrossRefGoogle Scholar
  78. Yúfera M, Pascual E, Polo A, Sarasquete MC (1993) Effect of starvation on the feeding ability of gilthead seabream (Sparus aurata L) larvae at first feeding. J Exp Mar Biol Ecol 16:259–272CrossRefGoogle Scholar
  79. Zambonino Infante JL, Cahu CL (1999) High dietary lipid levels enhance digestive tract maturation and improve Dicentrarchus labrax larval development. J Nutr 129:1195–1200CrossRefGoogle Scholar
  80. Zambonino Infante JL, Cahu CL (2001) Ontogeny of the gastrointestinal tract of marine fish larvae. Comp Biochem Physiol C: Toxicol Pharmacol 130(4):477–487Google Scholar
  81. Zambonino Infante JL, Gisbert E, Sarasquete S, Navarro I, Gutiérrez J, Cahu CL (2008) Ontogeny and physiology of the digestive system of marine fish larvae. In: JEP C, Bureau D, Kapoor BG (eds) Feeding and digestive functions in fishes. Science, Enfield, pp 281–348CrossRefGoogle Scholar

Copyright information

© Springer Nature B.V. 2018

Authors and Affiliations

  1. 1.AZTI Marine Research DivisionSukarrietaSpain
  2. 2.Grupo de Investigación en Acuicultura (GIA) Ecoaqua InstituteUniversidad de las Palmas de Gran CanariaTeldeSpain

Personalised recommendations