Abstract
A feeding experiment was conducted to investigate the effects of exogenous non-starch polysaccharide (NSP)-degrading enzymes in diets containing Gracilaria lemaneiformis (GL) on growth performance and digestive enzyme activities of white-spotted snapper Lutjanus stellatus Akazaki (initial mass 8.0 ± 0.1 g). A basal diet (D0) containing a mixed protein source (fish meal, soybean meal and GL meal) was used as the control. Two diets supplemented with 0.5 g (D1) and 1 g (D2) exogenous NSP-degrading enzymes per kilogram of diet were formulated. Each diet was assigned to triplicate groups of fish in a total of nine floating sea cages (270 fish, 30 fish per cage). After a 60-day feeding trail, significantly higher weight gain, specific growth ratio and feed efficiency ratio were observed in fish fed D2 diet compared to those of control (P < 0.05). Body lipid, moisture and ash contents were not significantly affected by NSP-degrading enzyme supplementation, but significantly higher protein content was noticed in fish fed D2 diet compared to that of control (P < 0.05). The amylase activity in the stomach and intestine was significantly higher in fish fed D2 diet (P < 0.05), but no significant differences were observed in pepsin and lipase activities in the stomach or trypsin and lipase activities in the intestine between all treatments. The results suggested that addition of 1 g kg−1 NSP-degrading enzymes in diet could efficiently improve seaweed feed utilization and growth performance of white-spotted snapper fish.
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Ai QH, Mai KS, Zhang WB, Xu W, Tan BP, Zhang CX, Li HT (2007) Effects of exogenous enzymes (phytase, non-starch polysaccharide enzyme) in diets on growth, feed utilization, nitrogen and phosphorus excretion of Japanese seabass, Lateolabrax japonicas. Comp Biochem Physiol A 147:502–508
Akazaki M (1983) A new lutjanid fish, Lutjanus stellatus, from southern Japan and a related species, L. rivulatus (Cuvier). Jpn J Ichthyol 29:365–373
Almirall M, Francesch M, Pérez-Vendrell AM, Brufau J, Esteve-García E (1995) The differences in intestinal viscosity produced by barley and s-glucanase alter digesta enzyme activities and ileal nutrient digestibilities more in broiler chicks than in cocks. J Nutr 125:947–955
Angkanaporn K, Choct M, Bryden WL, Annison EF, Annison G (1994) Effects of wheat pentosans on endogenous amino acid losses in chickens. J Sci Food Agric 66:399–404
Association of Official Analytical Chemists (AOAC) (2009) Official methods of for analysis. Gaithersburg, Maryland. http://www.eoma.aoac.org/. Cited 14 Mar 2012
Bach-Knudsen KE (1997) Carbohydrate and lignin contents of plant materials used in animal feeding. Anim Feed Sci Technol 67:319–338
Bdeford MR (1995) Mechanism of action and potential environmental benefits from the use of feed enzymes. Anim Feed Sci Technol 53:145–155
Borquez A, Serrano E, Dantagnan P, Carrasco J, Hernandez A (2011) Feeding high inclusion of whole grain white lupin (Lupinus albus) to rainbow trout (Oncorhynchus mykiss): effects on growth, nutrient digestibility, liver and intestine histology and muscle fatty acid composition. Aquac Res 42:1067–1078
Carter CG, Hauler RC (2000) Fishmeal replacement by plant meals in extruded feeds for Atlantic salmon, Salmo salar L. Aquaculture 185:299–311
Casas VM, Portillo CG, Aguila RN, Rodríguez AS, Sánchez RI, Carrillo DS (2006) Effect of the marine algae Sargassum spp. on the productive parameters and cholesterol content of the brown shrimp, Farfantepenaeus californiensis (Holmes, 1900). Rev Biol Mar Oceanogr 41:97–105
Chesson A (1993) Feed enzyme. Anim Feed Sci Technol 45:65–79
Classen HL (1996) Cereal grain starch and exogenous enzymes in poultry diets. Anim Feed Sci Technol 62:21–27
Cowieson AJ, Singh DH, Adeola O (2006) Prediction of ingredient quality and the effect of a combination of xylanase, amylase, protease and phytase in the diets of broiler chicks. 1. Growth performance and digestible nutrient intake. Br Poult Sci 47:477–489
Danicke S, Simon O, Jeroch H (2003) Effects of dietary fat type and non-starch polysaccharide hydrolysing enzyme addition to rye-based diets on muscle protein turnover in broilers. Br Poult Sci 44:245–255
Davies SJ, Brown MT, Camilleri M (1997) Preliminary assessment of the seaweed Porphyra purpurea in artificial diets for thick-lipped grey mullet (Chelon labrosus). Aquaculture 152:249–258
Dudley-Cash WA (1997) NSP: a simple classification for a complex group of chemicals. Feed Stuffs 69:11
Fei XG, Bao Y, Lu S (1999) Seaweed cultivation: traditional way and its reformation. Chin J Oceanol Limnol 7:193–199 (In Chinese with English Abstract)
Francis G, Makkar HPS, Becker K (2001) Antinutritional factors present in plant derived alternate fish feed ingredients and their effects in fish. Aquaculture 199:197–227
Gdala J, Johansen HN, Bach Knudsen KE, Knap IH, Wagner P, Jørgensen OB (1997) The digestibility of carbohydrates, protein and fat in the small and large intestine of piglets fed non-supplemented and enzyme supplemented diets. Anim Feed Sci Technol 65:15–33
Glencross BD, Booth M, Allan GL (2007) A feed is only as good as its ingredients—a review of ingredient evaluation strategies for aquaculture feeds. Aquac Nutr 13:17–34
Glencross B, Rutherford N, Bourne N (2012) The influence of various starch and non-starch polysaccharides on the digestibility of dies fed to rainbow trout (Oncorhynchus mykiss). Aquaculture 356–357:141–146
Govoni JJ, Boehlert GW, Watanabe Y (1986) The physiology of digestion in fish larvae. Environ Biol Fishes 16:59–77
Guillaume J, Métailler R (2001) Antinutritional factors. In: Guillaume J, Kaushik S, Bergot P, Métailler R (eds) Nutrition and feeding of fish and crustaceans. Springer Praxis Publishing, Chichester, pp 297–307
Hardy RW (2010) Utilization of plant proteins in fish diets: effects of global demand and supplies of fishmeal. Aquac Res 41:770–776
Hardy RW, Barrows FT (2002) Diet formulation and manufacture. In: Halver JE, Hardy RW (eds) Fish nutrition, 3rd edn. Academic Press, San Diego, pp 505–600
Iversen M, Finstad B, McKinley RS, Eliassen RA (2003) The efficacy of metomidate, clove oil, Aqui-STM and Benzoak as anaesthetics in Atlantic salmon (Salmo salar L.) smolts, and their potential stress-reducing capacity. Aquaculture 221:549–566
Jamroz D, Jakobsen K, Knudsen KEB, Wiliczkiewicz A, Orda J (2002) Digestibility and energy value of non-starch polysaccharides in young chickens, ducks and geese, fed diets containing high amounts of barley. Comp Biochem Physiol A 131:657–668
Jobling M (1994) Fish bioenergetics. Chapman and Hall, London, p 309
Kaushik SJ, Cravedi JP, Lalles JP, 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
Kaushik SJ, Covès D, Dutto G, Blanc D (2004) Almost total replacement of fish meal by plant protein sources in the diet of a marine teleost, the European seabass, Dicentrarchus labrax. Aquaculture 230:391–404
Kolkovski S, Tandler A, Kissil GW, Gertler A (1993) The effect of dietary exogenous digestive enzymes on ingestion, assimilation, growth and survival of gilthead seabream (Sparus aurata, Sparidae, Linnaeus) larvae. Fish Physiol Biochem 12:203–209
Kraugerud OF, Penn M, Storebakken T, Refstie S, Krogdahl A, Svihus B (2007) Nutrient digestibilities and gut function in Atlantic salmon (Salmo salar) fed diets with cellulose or non-starch polysaccharides from soy. Aquaculture 273:96–107
Krogdahl A, Hemre GI, Mommsen TP (2005) Carbohydrates in fish nutrition: digestion and absorption in post larval stages. Aquac Nutr 11:103–122
Kumar S, Sahu NP, Pal AK, Choudhury D, Mukherjee SC (2006) Studies on digestibility and digestive enzyme activities in Labeo rohita (Hamilton) juveniles: effect of microbial α-amylase supplementation in non-gelatinized or gelatinized corn-based diet at two protein levels. Fish Physiol Biochem 32:209–220
Li JS, Li JL, Wu TT (2009) Effects of non-starch polysaccharide enzyme, phytase and citric acid on activities of endogenous digestive enzymes of tilapia (Oreochromis niloticus × Oreochromis aureus). Aquac Nutr 15:415–420
Lovell RT (2002) Diet and fish husbandry. In: Halver JE, Hardy RW (eds) Fish nutrition. Academic Press, San Diego, pp 703–754
Lowry OH, Rosebrough NJ, Farr AL, Randall RJ (1951) Protein measurement with the Folin-phenol reagent. J Biol Chem 193:265–275
Mohamed S, Hashim SN, Rahman HA (2012) Seaweeds: a sustainable functional food for complementary and alternative therapy. Trends Food Sci Technol 23:83–96
Nakagawa H, Umino T, Tasaka Y (1997) Usefulness of Ascophyllum meal as a feed additive for red sea bream, Pagrus major. Aquaculture 151:275–281
Papatryphon E, Howell RA, Soares JJH (1999) Growth and mineral absorption by striped bass Morone saxatilis fed a plant feedstuff based diet supplemented with phytase. J World Aquac Soc 30:161–173
Pettersson D, Åman P (1989) Enzyme supplementation of a poultry diet containing wheat and rye. Br J Nutr 62:139–149
Refstie S, Svihus B, Shearer KD, Storebakken T (1999) Nutrient digestibility in Atlantic salmon and broiler chickens related to viscosity and non-starch polysaccharide content in different soyabean products. Anim Feed Sci Technol 79:331–345
Refstie S, Sahlstrom S, Brathen 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
Robaina L, Izquierdo MS, Moyano FJ, Socorro J, Vergara JM, Montero D, Fernández PH (1995) Soybean and lupin seed meals as protein sources in diets for gilthead seabream (Sparus aurata). Nutritional and histological implications. Aquaculture 130:219–233
Rupérez P, Saura CF (2001) Dietary fibre and physicochemical properties of edible Spanish seaweeds. Eur Food Res Technol 212:349–354
Shao KT, Ho HC, Lin PL, Lee PF, Lee MY, Tsai CY, Liao YC, Lin YC, Chen JP, Yeh HM (2008) A checklist of fishes of southern Taiwan, northern South China sea. Raffles Bull Zool 19:233–271
Storebakken T, Shear KD, Roem AJ (1998) Availability of protein, phosphorus and other elements in fishmeal, soy-protein concentration and phytase treated soy protein concentrate based diets to Atlantic salmon (Salmo salar). Aquaculture 161:365–379
Tacon AGJ, Hasan MR, Metian M (2011) FAO fisheries and aquaculture technical paper, 564
Tseng CK (2001) Algal biotechnology industries and research activities in China. J Appl Phycol 13:375–380
Valente LMP, Gouveia A, Rema P, Matos J, Gomes EF, Sousa-Pinto I (2006) Evaluation of three seaweeds Gracilaria bursa-pastoris, Ulva rigida and Gracilaria cornea as dietary ingredients in European sea bass (Dicentrarchus labrax) juveniles. Aquaculture 252:85–91
Wahbeh MI (1997) Amino acid and fatty acid profiles of four species of macroalgae from Aqaba and their suitability for use in fish diets. Aquaculture 159:101–109
Wang CY, Shan SS, Xu SA (2012) Preliminary study on enzymolysis of non-starch polysaccharide in feed seaweed powder using pre-digestion method. Feed Ind 33:44–48 (In Chinese with English Abstract)
Wassef EA, Masry MHE, Mikhail FR (2001) Growth enhancement and muscle structure of striped mullet, Mugil cephalus L., fingerlings by feeding algal meal-based diets. Aquac Res 32(S1):315–322
Watanabe T, Pongmaneerat J (1993) Potential of soybean meal as a protein source in extruded pellets for rainbow trout. Nippon Suisan Gakkaishi 59:1415–1423
Xuan XZ, Wen XB, Li SK, Zhu DS, Li YY (2013) Potential use of macro-algae Gracilaria lemaneiformis in diets for the black sea bream, Acanthopagrus schlegelii, juvenile. Aquaculture 412–413:167–172
Yu J, Wang X, Chen MZ, Zhang YY, Long ZJ (2006) Analysis on nutritional components and polysaccharide composition of Gracilaria lemaneiformis from Chaoshan Coast. Food Sci 27:93–96 (In Chinese with English Abstract)
Zhang L, Mai KS, Ai QH, Tan BP (2006) Effects of phytase and non-starch polysaccharide enzyme supplementation in diets on growth and digestive enzyme activity in large yellow croaker, Pseudosciaena crocea R. Periodic Ocean Univ China 36:923–928 (In Chinese with English Abstract)
Zhang L, Ai QH, Mai KS, Li J, Li HT, Zhang CX, Zheng SX (2009) Effects of phytase and non-starch polysaccharide enzyme supplementation in diets on growth and digestive enzyme activity for Japanese seabass, Lateolabrax Japonicus C. Acta Hydrobiol Sin 33:82–88 (In Chinese with English Abstract)
Acknowledgments
This study was supported by Grant Nos. 41276179 and 41276179 from National Natural Science Foundation of China, Grant No. S2011030005257 from Guangdong Natural Science Foundation and Grant No. 2010B020201015 from Guangdong Science and Technology Funding Scheme, and the authors thank Prof. Chiju Wei, of the College of Science, Shantou University, China, for reviewing the manuscript and his helpful suggestions.
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Zhu, D., Wen, X., Li, S. et al. Effects of exogenous non-starch polysaccharide-degrading enzymes in diets containing Gracilaria lemaneiformis on white-spotted snapper Lutjanus stellatus Akazaki. Aquacult Int 24, 491–502 (2016). https://doi.org/10.1007/s10499-015-9940-5
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DOI: https://doi.org/10.1007/s10499-015-9940-5