Effects of dietary vegetable oils on liver and gonad fatty acid metabolism and gonad maturation in gilthead seabream (Sparus aurata) males and females
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Abstract
A 20-week growth trial was conducted to investigate the effect of two dietary blended vegetable oils (VO) on liver lipogenic enzyme activity, liver and gonad lipid class composition and fatty acid profiles, serum sex hormones, and gonad morphohistology in gilthead seabream, Sparus aurata. Three groups of fish (BW i 130.9 ± 3.1 g) were fed, close to satiation, three experimental diets: a control (CTRL) contained fish oil (FO) as the sole lipid source (100% FO) and two VO-blended diets in each 60% of FO was substituted by an equal mixture of cottonseed oil (CO), sunflower oil (SFO) and either linseed oil (LO) or soybean oil (SBO), designated as LO or SBO diet, respectively. Each diet was assigned to triplicate groups of fish. Results showed that all dietary treatments presented no significant (P > 0.05) differences in growth rate and feed conversion ratio for sexes combined. Enzyme activities of liver lipogenic enzymes of LO-fed fish (glucose-6-phosphate dehydrogenase (G6PDH), malic enzyme (ME) and fatty acid synthetase (FAS)) were not statistically (P > 0.05) different from those of CTRL fish. Only in the group of fish fed the SBO diet, G6PDH was slightly higher (P < 0.05) for both sexes, while ME showed a significant (P < 0.05) higher activity only in females relative to CTRL fish. Liver FAS enzyme activity remained unaltered among dietary groups. VO-fed fish recorded a significant (P < 0.05) increase in total lipid (TL) and triglyceride (TAG) contents in both liver and gonad, more pronounced in females than in males, concurrent with a significant (P < 0.05) decrease in cholesterol (CHL) and phospholipids (PL), more obvious for the SBO-fed fish, as compared to CTRL. The fatty acid (FA) composition of liver or gonad reflected that of the supplied diet and evidenced a significant (P < 0.01 or <0.05) alteration in the majority of individual FA in VO-fed fish compared to CTRL. There were decreased levels of ARA (20:4 n-6), EPA (20:5 n-3), and DHA (22:6 n-3) in VO-fed fish, more pronounced in females than in males, compared to CTRL. The liver and gonad FA profiles, for males and females, reflected the composition of the diet and showed sex variation in the output of multivariate principal component analysis (PCA). Feeding fish VO diets has also led to a significant (P < 0.05) reduction in serum estradiol level by 15.8 or 22.3% in LO- or SBO-fed fish, respectively, and in testosterone level by 7.7% in the latter dietary group only compared to the CTRL. Histomorphological examination of ovary and testis has indicated a relative retardation in oogenesis and spermatogenesis in VO-fed fish, less obvious in the LO-fed fish compared to CTRL. These results suggest a preference of LO over SBO blend diet in terms of liver lipogenic enzyme activity, liver and gonad lipid content, lipid class composition and fatty acid profile, serum sex hormones as well as gonad maturation. PCA analysis of gonads highlighted the importance of using a 100% marine FO diet for gilthead seabream broodstock for the recovery of a normal FA profile in gonads of fish, previously fed VO over the production cycle, to ensure successful spawning.
Keywords
Gilthead seabream Linseed oil Soybean oil Liver lipogenic enzymes Lipid classes Sex hormones Gonad histologyAbbreviations
- FO
Fish oil
- VO
Vegetable oil
- CO
Cottonseed oil
- SFO
Sunflower oil
- LO
Linseed oil
- SBO
Soybean oil
- CTRL
Control
- TL
Total lipids
- FA
Fatty acids
- SFA
Saturated fatty acids
- MUFA
Monounsaturated fatty acids
- PUFA
Polyunsaturated fatty acids
- HUFA
Highly unsaturated fatty acids
- ARA
Arachidonic acid
- EPA
Eicosapentaenoic acid
- DHA
Docosahexaenoic acid
- LA
Linoleic acid
- LNA
Linolenic acid
- OA
Oleic acid
- PGs
Prostaglandins
- TAG
Triglycerides
- PL
Phospholipids
- CHL
Cholesterol
- TLC
Thin-layer chromatography
- GLC
Gas liquid chromatography
- FAME
Fatty acid methyl ester
- G6PDH
Glucose-6-phosphate dehydrogenase enzyme
- ME
Malic enzyme
- FAS
Fatty acid synthetase
- H and E
Hematoxylin and eosin
- A and B
Spermatogonia
- C
Primary spermatocytes
- D
Secondary spermatocytes
- E
Spermatids
- PO
Perinucleolus oocyte
- CA
Cortical alveoli
- PY
Primary yolk oocytes
- SY
Secondary yolk oocytes
Notes
Acknowledgments
The authors are very grateful to Dr Fady R. Mickaeel, Fish Nutrition Laboratory, National Institute of Oceanography and Fisheries, Alexandria, for the help he kindly offered in the statistical analysis of data. Sincere thanks are also due to this article reviewer for his valuable comments that greatly helped in improving the final presentation.
References
- Almansa E, Martin MV, Cejas JR, Badía P, Jerez S, Lorenzo A (2001) Lipid and fatty acid composition of female gilthead seabream during their reproductive cycle: effects of a diet lacking n-3HUFA. J Fish Biol 59:267–286CrossRefGoogle Scholar
- AOAC (1995) Association of official analytical chemists. Official Methods of Analysis, Washington DCGoogle Scholar
- Asturiano JF, Sorbera LA, Carrillo M, Zanuy S, Ramos J, Navarro JC, Bromage N (2001) Reproductive performance in male European Seabass (Dicentrarchus labrax, L.) fed two PUFA-enriched experimental diets: a comparison with males fed a wet diet. Aquaculture 194(1–2):173–190CrossRefGoogle Scholar
- Bell JG, Sargent JR (2003) Arachidonic acid in aquaculture feeds: current status future opportunities. Aquaculture 218:491–499CrossRefGoogle Scholar
- Bell JG, McEvoy Y, Tocher DR, McGhee F, Campbell PJ, Sargent JR (2001) Replacement of fish oil with rapeseed oil in diets of Atlantic salmon (Salmo salar) affects tissues lipid compositions and hepatocyte fatty acid metabolism. J Nutr 131:1535–1543PubMedGoogle Scholar
- Bell JG, McGhee F, Dick JR, Tocher DR (2005) Dioxin and dioxin-like polychlorinated (PCBs) in Scottish farmed salmon (Salmo salar): effects of replacement of dietary marine fish oil with vegetable oils. Aquacult Res 37:606–617CrossRefGoogle Scholar
- Benedito-Palos L, Navarro JC, Sitjá-Bobadilla A, Bell JG, Kaushik SJ, Pérez-Sánchez J (2008) High levels of vegetable oils in plant protein-rich diets fed to gilthead bream (Sparus aurata L.): growth performance, muscle fatty acid profiles and histological alterations of target tissues. Brit J Nutr 100:992–1003PubMedCrossRefGoogle Scholar
- Benedito-Palos L, Navarro JC, Kaushik SJ, Pérez-Sánchez J (2010) Tissue-specific robustness of fatty acid signature in cultured gilthead seabream (Sparus aurata L.) fed practical diets with a combined high replacement of fish meal and fish oil. J Anim Sci 88:1759–1770PubMedCrossRefGoogle Scholar
- Benedito-Palos L, Bermejo-Nogales A, Karampatos AI, Navarro JC, Diez A, Bautista JM, Bell JG, Tocher DR, Obach A, Kaushik SJ, Pérez-Sánchez J (2011) Modelling the predictable effects of dietary lipid sources on the fillet fatty acid composition on one-year-old gilthead seabream (Sparus aurata L.). Food Chem 124:538–544CrossRefGoogle Scholar
- Bouraoui L, Sánchez-Gurmaches J, Cruz-Garcia L, Gutrẻrrez J, Benedito-Palos L, Pẻrez-Sánchez J, Navarro JC (2010) Effect of dietary fish meal and fish oil replacement on lipogenic and lipoprotein lipase activities and plasma insulin in gilthead seabream (Sparas aurata L.). Aquacult Nutr. doi: 10.1111/j.1365-2095.2009.00706.x
- Bruce M, Oyen F, Bell G, Austuriano JF, Farndale B, Ramos J, Bromage N, Carrillo M, Zanuy S (1999) Development of broodstock diets for the European seabass (Dicentrarchus labrax) with special emphasis on the importance of n-3 and n-6 HUFA to reproductive performance. Aquaculture 177:85–97CrossRefGoogle Scholar
- Caballero MJ, Izquierdo MS, Kjorsvik E, Fernandez AJ, Rosenlund G (2004) Histological alterations in the liver of seabream Sparus aurata, caused by short- or long term feeding with vegetable oils: recovery of normal morphology after feeding fish oil as the sole lipid source. J Fish Dis 27:531–541PubMedCrossRefGoogle Scholar
- Cejas JR, Almansa E, Villamandos JE, Badia P, Bolanos A, Lorenzo A (2004) Lipid and fatty acid composition of ovaries from wild fish and ovaries and eggs from captive fish of white seabream (Diplodus sargus). Aquaculture 216:299–313CrossRefGoogle Scholar
- Cerdá J, Zanuy S, Carrillo M (1997) Evidence for dietary effects on plasma levels of sexual steroids during spermatogenesis in the seabass. Aquaculture Int 5:473–477CrossRefGoogle Scholar
- Christie WW (1982) Lipid analysis. In: Christie WW (ed) Lipid analysis, 2nd edn. Perganon Press, Oxford, pp 17–23 (51–61)Google Scholar
- Diaz-Lopez M, Perez MJ, Acosta NG, Tocher DR, Jerez S, Lorenzo A, Rodriguez C (2009) Effect of dietary substitution of fish oil by Echium oil on growth, plasma parameters and body lipid composition in gilthead seabream (Sparus aurata L.). Aquac Nutr 15:500–512CrossRefGoogle Scholar
- Fernández-Palacios H, Izquierdo MS, Robaina L, Valencia A, Salhi M, Vergara J (1995) Effect of n-3 HUFA level in brood stock diets on egg quality of gilthead seabream (Sparus aurata L.). Aquaculture 132:325–337CrossRefGoogle Scholar
- Figueiredeo-Silva A, Rocha E, Dias J, Silva P, Rema P, Gomes E, Valente LMP (2005) Partial replacement of fish oil by soybean oil on lipid distribution and liver histology in European seabass (Dicentrarchus labrax) and rainbow trout (Oncorhynchus mykiss) juveniles. Aquac Nutr 11:147–155CrossRefGoogle Scholar
- Folch J, Lee M, Sloan-Stanley GH (1957) A simple method for the isolation and purification of total lipids from animal tissues. J Biol Chem 226:497–509PubMedGoogle Scholar
- Garcia-Rejỏn L, Sanchez-Muros MJ, Cerdá J, de la Higuera M (1997) Fructose 1, 6 biphosphate activity in liver and gonads of seabass (Dicentrarchus labrax): influence of diet composition and stage of the reproductive cycle. Fish Physiol Biochem 16(2):93–105CrossRefGoogle Scholar
- Hammoud V, Saad A (2007) Reproductive biology of Diplodus vulgaris (Family Sparidae) on the Syrian coast. Rapp Comm Int Mer Mẻdit 38:495–503Google Scholar
- Harel M, Tandler A, Kissil GW (1994) The kinetics of nutrient incorporation into body tissues of gilthead seabream (Sparus aurata) females and the subsequent effects on eggs composition and egg quality. Br J Nutr 72:4–48CrossRefGoogle Scholar
- Izquierdo MS (2005) Essential fatty acid requirements in Mediterranean fish species. Cahier Options Méditerranéennes. Mediterr Fish Nut 63:91–102Google Scholar
- Izquierdo MS, Fernandez-Palacios H, Tacon AG (2001) Effect of broodstock nutrition on reproductive performance of fish. Aquaculture 197:25–42CrossRefGoogle Scholar
- Izquierdo MS, Obach A, Arantzamendi L, Montero D, Robaina L, Rosenlund G (2003) Dietary lipid sources for seabream and seabass: growth performance, tissue composition and flesh quality. Aquacul Nutr 9:397–407CrossRefGoogle Scholar
- Juaneda P, Rocquelin G (1985) Rapid and convenient separation of phospholipids and non-phosphorus lipids from heart using silica cartridges. Lipids 20:40–48PubMedCrossRefGoogle Scholar
- Kime DE (1993) Classical and non-classical steroids in teleost fish. Rev Fish Biol Fish 3:160–180CrossRefGoogle Scholar
- Koven WM, Tandler A, Sklan D, Kissil GWM (1992) The association of eicosapentaenoic and docosahexaenoic acids in the phospholipids of different age Sparus aurata larvae with growth. Aquaculture 116:71–82CrossRefGoogle Scholar
- Lin H, Romsos DL, Tack PI, Leveille GA (1997) Effects of fasting and feeding various diets on hepatic lipogenic enzyme activities in coho salmon (Oncorhynchus kisutch Walbaum). J Nutr 107:1477–1483Google Scholar
- Martin MV, Rodriguez C, Cejas JR, Perez MJ, Jerez S, Lorenzo A (2008) Body lipid and fatty acid composition in male gilthead seabream broodstock at different stages of the reproductive cycle: effects of a diet lacking n-3 and n-6 HUFA. Aquac Nutr 14:1–13Google Scholar
- Matsayama M, Takenchi H, Keifi-Hivose K, Kagawa H (1995) Induced gonadal development and spawning of immature Red seabream Pagrus major with LHRH-a administration in different ways during winter season. Fisheries Science 61(3):472–477Google Scholar
- Menoyo D, Izquierdo MS, Robaina L, Ginés R, Lopez-Bote CJ, Bautista JM (2004) Adaptation of lipid metabolism, tissue composition and flesh quality in gilthead seabream (Sparus aurata) to the replacement of dietary fish oil by linseed and soybean oils. Brit J Nutr 92:41–52PubMedCrossRefGoogle Scholar
- Montero D, Robaina I, Caballero R, R Ginés, Izquerdo MS (2005) Growth, feed utilization and flesh quality of European seabass (Dicentrarchus labrax L.) fed diets containing vegetable oils: a time-course study on the effect of a re-feeding period with a 100% fish oil diet. Aquaculture 248:121–134CrossRefGoogle Scholar
- Mourente G, Good JE, Bell JG (2005) Partial substitution of fish oil with rapeseed, linseed and olive oils in diets for European seabass (Dicentrarchus labrax L.): effects on flesh fatty acid composition, plasma prostaglandins E2 and F2α, immune function and effectiveness of a fish oil finishing diet. Aquacul Nutr 11:25–40CrossRefGoogle Scholar
- Ogata HY, Ogata AC, Emata ES, Furuita H (2004) Fatty acid composition of five candidate aquaculture species in central Philippines. Aquaculture 236:361–375CrossRefGoogle Scholar
- Richard N, Mourente G, Kaushik S, Corraze G (2006a) Replacement of a large portion of fish oil by vegetable oils does not affect lipogenesis, lipid transport and tissue lipid uptake in European seabass (Dicentrarchus labrax L.) Aquaculture 261(3):1077–1087Google Scholar
- Richard N, Kaushik S, Larroquet L, Panserat S, Corraze G (2006b) Replacing dietary fish oil by vegetable oils has little effects on lipogenesis, lipid transport and tissue lipid up take in rainbow trout (Oncorhynchus mykiss). Br J Nutr 96:299–309PubMedCrossRefGoogle Scholar
- Rodriguez C, Perez JA, Diaz M, Izquierdo MS, Fernandez-Palacios H, Lorenzo HA (1997) Influence of the EPA/DHA ratio in rotifers on gilthead seabream (Sparus aurata) larval development. Aquaculture 150:77–89CrossRefGoogle Scholar
- Sargent JR (1995) Origin and functions of egg lipids: nutritional implications. In: Bromage NR, Roberts RJ (eds) Broodstock management and egg and larval quality. Blackwell, London, pp 353–372Google Scholar
- Sargent JR, Bell MV, Tocher DR (1993) Docosahexaenoic acid and development of brain and retina in marine fish. In: Drevon CA, Baksaas I, Krokan HE (eds) Omega-2 fatty acids: metabolism and biological effects. Birkhauser, Basel, pp 139–149Google Scholar
- Shimeno S, Hosokawa H, Takeda M, Takayama S, Fukui A, Sasaki H (1981) Adaptation of hepatic enzymes to dietary lipid in young yellow tail. Nippon Suisan Gakkaishi 47:63–69CrossRefGoogle Scholar
- Silverstein JT, Shimma H, Ogata H (1997) Early maturity in amago salmon (Oncorhynchus masu ishikawai) an association with energy storage. Can J Fish Aquat Sci 54:444–451CrossRefGoogle Scholar
- Sorbera LA, Asturiano JF, Carrillo M, Zanuy S (2001) Effects of polyunsaturated fatty acids and prostaglandins on oocyte maturation in a marine teleost, the European seabass (Dicentrarchus labrax). Biol Reprod 64:382–389PubMedCrossRefGoogle Scholar
- Tocher DR, Harvie DG (1988) Fatty acid composition of the major phosphoglycerides from fish neural tissue (n-3) and (n-6) polyunsaturated fatty acids in rainbow trout (Salmo gairdneri L.) and cod (Gadus morhua) brains and retinas. Fish Physiol Biochem 5:229–239CrossRefGoogle Scholar
- Torstensen BE, Frǿyland L, Lie Ø (2004) Replacing dietary fish oil with increasing levels of rapeseed oil and olive oil-effects on Atlantic salmon (Salmo salar L.) tissue and lipoprotein composition and lipogenic enzyme activities. Aquacul Nutr 10:175–192CrossRefGoogle Scholar
- Turchini GM, Torstensen BE, Ng WK (2009) A review: fish oil replacement in finfish nutrition. Rev Aqua 1:10–57CrossRefGoogle Scholar
- Wade MG, Van Der Kraak G, Gerrits MF, Ballautyne JS (1994) Release and steroidogenic actions of polyunsaturated fatty acids in the gold fish testis. Biol Reprod 5l:131–139CrossRefGoogle Scholar
- Wassef EA (1985) Reproduction of gilthead seabream, Sparus aurata, L. (Sparidae) in the Egyptian Mediterranean waters off Alexandria. J Egypt Vet Ass 45(1):25–39Google Scholar
- Wassef EA, Wahby OM, Sakr EM (2007) Effect of dietary vegetable oils on health and liver histology of gilthead seabream (Sparus aurata) growers. Aquaculture Res 38:852–861CrossRefGoogle Scholar
- Wassef EA, Saleh NE, Abdel-Hady HA (2009) Vegetable oil blend as alternative lipid resources in diets for gilthead seabream, Sparus aurata. Aquacul Int 17:421–435CrossRefGoogle Scholar
- Watanabe T, Vassalio-Aguis R (2003) Brood stock nutrition research on marine fish in Japan. Aquaculture 227:35–61CrossRefGoogle Scholar
- West G (1990) Methods of assessing ovarian development in fishes. Aust J Mar Freshw Res 41:199–222CrossRefGoogle Scholar
- Zerez S, Rodriguez C, Cejas JR, Bolanos A, Lorenzo A (2006) Lipid dynamics and plasma level changes of 17β-estradiol and testosterone during the spawning season of gilthead seabream (Sparus aurata) females of different ages. Comp Biochem Physiol 143(B):180–189Google Scholar
- Zhou QB, Wu HD, Zhu CS, Yan XH (2010) Effects of dietary lipids on tissue fatty acids profile, growth and reproductive performance of female rice field eel (Monopterus albus). Fish Physiol Biochem. doi: 10.1007/s10695-010-9444-1