Skip to main content
Log in

The green alga Ulva lactuca as a potential ingredient in diets for juvenile white spotted snapper Lutjanus stellatus Akazaki

  • Published:
Journal of Applied Phycology Aims and scope Submit manuscript

Abstract

This trial evaluated the green alga Ulva lactuca as a potential ingredient in diets for juvenile white-spotted snapper Lutjanus stellatus Akazaki (initial mass 12.10 ± 0.10 g). Five test diets had similar protein and lipid levels (42 % crude protein and 8.5 % crude lipid), control diet without U. lactuca meal, four diets were added 5, 10, 15, and 20 % U. lactuca meal to investigate the effects of U. lactuca on growth performance, carcass composition, and enzyme activities of the fish. Each diet was assigned to triplicate groups of 30 fish for 60 days in 15 floating sea cages. At the end of feeding trail, final body weight (FBW), weight gain (WG), specific growth rate (SGR) of the fish fed 5 % UL diet were significantly higher than that of 10 and 20 % groups (P < 0.05). Pepsin activities in the stomach were significantly suppressed for the fish received 20 % U. lactuca diet (P < 0.05), lipase activity in stomach and intestinal decreased with increasing U. lactuca inclusion level in diet. The enzyme activities of aspartate amino transferase (AST) in liver and alanine amino transferase (ALT) in serum increased significantly from 5 to 20 % U. lactuca level (P < 0.05). These results indicate that incorporation of the U. lactuca in the diet at 5 % for juvenile white spotted snapper does beneficial effects on the growth performance but higher level of incorporation reduce fish performance and physiological state.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Similar content being viewed by others

References

  • Adhikari S, Sarkar B, Chatterjee A, Mahapatra CT, Ayyappan S (2004) Effects of cypermethrin and carbofuran on certain haematological parameters and prediction of their recovery in a freshwater teleost, Labeo rohita (Hamilton). Ecotoxicol Environ Saf 58:220–226

    Article  CAS  PubMed  Google Scholar 

  • 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

    Google Scholar 

  • AOAC (Association of Official Analytical Chemists) (1999) Official Methods of Analysis of the Association of Official Analytical Chemists. Washington D.C.

  • Barton BA, Morgan JD, Vijayan MM (2002) Physiological and condition-related indicators of environmental stress in fish. In: Adams SM (ed) Biological indicators of aquatic ecosystem stress. American Fisheries Society, Bethesda, pp 111–148

    Google Scholar 

  • 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. Aquacult Res 42:1067–1078

    Article  CAS  Google Scholar 

  • Brinker A (2009) Improving the mechanical characteristics of faecal waste in rainbow trout: the influence of fish size and treatment with a non-starch polysaccharide (guar gum). Aquacult Nutr 15:229–240

    Article  CAS  Google Scholar 

  • Casas-Valdez M, Portillo-Clark G, Aguila-Ramírez N, Rodríguez-Astudillo S, Sánchez-Rodríguez I, Carrillo-Domínguez S (2006) Effect of the marine algae Sargassum spp. on the productive parameters and cholesterol content of the green shrimp, Farfantepenaeus californiensis (Holmes, 1900). Rev Biol Mar Oceanogr 41:97–105

    Article  Google Scholar 

  • Chandini SK, Ganesan P, Bhaskar N (2008) In vitro antioxidant activities of three selected green seaweeds of India. Food Chem 107:707–713

    Article  CAS  Google Scholar 

  • Davies SJ, Green 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

    Article  Google Scholar 

  • Drew MD, Borgeson TL, Thiessen DL (2007) A review of processing of feed ingredients to enhance diet digestibility in finfish. Anim Feed Sci Technol 138:118–136

    Article  CAS  Google Scholar 

  • FAO (2010) Fisheries and Aquaculture Information and Statistics Service, Aquaculture production: quantities 1950-2008, FISHSTAT Plus—Universal Software for Fishery Statistical Time Series [Online or CD-ROM], Food and Agriculture Organization of the United Nations, Available at: http://www.fao.org/fi/statist/FISOFT/FISHPLUS.asp

  • FAO (2011) Fish stat Plus: Universal software for fishery statistical time series. Aquaculture production: quantities 1950-2009; aquaculture production: values 1984-2009; capture production: 1950-2009; commodities production and trade: 1950-2008; total production: 1970-2009, Vers. 2.30. Available at. FAO Fisheries Department, Fishery Information, Data and Statistics Unit. http:// www.fao.org/fi/statist/FISOFT/FISHPLUS.asp

  • FAO (2012) Feeding the Growth Aquaculture Sector: An Analysis. Sixth Session of the Sub-Committee on Aquaculture. Committee on Fisheries, Cape Town

    Google Scholar 

  • Fleurence J (1999) Seaweed proteins: biochemical nutritional aspects and potential uses. Trends Food Sci Technol 10:25–28

    Article  CAS  Google Scholar 

  • Fleurence J (2004) Seaweed proteins. In: Yada RY (ed) Proteins in food processing. Woodhead Publishing, Cambridge, pp 197–213

    Chapter  Google Scholar 

  • Fleurence J, Chenard E, Luçon M (1999) Determination of the nutritional value of proteins obtained from Ulva armoricana. J Appl Phycol 11:231–239

    Article  CAS  Google Scholar 

  • Folmar LC, Moody T, Bonomelli S, Gibson J (1992) Annual cycle of blood chemistry parameters in striped mullet (Mugil cephalus L.) and pinfish (Lagodon rhomboides L.) from the Gulf of Mexico. J Fish Biol 41:999–1011

    Article  CAS  Google Scholar 

  • Francis G, Makkar HP, Becker K (2001) Antinutritional factors present in plant derived alternate fish feed ingredients and their effects in fish. Aquaculture 199:197–227

    Article  CAS  Google Scholar 

  • Glencross BD, Booth M, Allan GL (2007) A feed is only as god as its ingredients—a review of ingredient evaluation strategies for aquaculture feeds. Aquacult Nutr 13:17–34

    Article  CAS  Google Scholar 

  • 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

    Google Scholar 

  • Guo TT, Xu HL, Zhang LX (2007) In vivo protective effect of Porphyra yezoensis polysaccharide against carbon tetrachloride induced hepatotoxicity in mice. Regul Toxicol Pharmacol 49:101–106

    Article  CAS  PubMed  Google Scholar 

  • Hardy RW (1996) Alternate protein sources for salmon and trout diets. Anim Feed Sci Technol 59:71–80

    Article  Google Scholar 

  • Hardy RW (2010) Utilization of plant proteins in fish diets: effects of global demand and supplies of fishmeal. Aquacult Res 41:770–776

    Article  CAS  Google Scholar 

  • Hardy RW, Barrows FT (2002) Diet formulation and manufacture. In: Halver JE, Hardy RW (eds) Fish Nutrition, 3rd edn. Academic Press, NY, pp 505–600

    Google Scholar 

  • Horie Y, Sugase K, Horie K (1995) Physiological difference of soluble and insoluble dietary fibre fractions of green algae and mushrooms in pepsin activity in vitro and protein digestibility. Asia Pac J Clin Nutr 4:251–255

    CAS  PubMed  Google Scholar 

  • Huang ZG (1994) The species and distribution of marine organisms. Ocean Press, Beijing, pp 201–232 (in Chinese)

    Google Scholar 

  • Indegaard M, Minsaas J (1991) Seaweed Resources in Europe. Uses and Potential. In: Guiry MD, Blunden G (eds) Animal and Human Nutrition. John Wiley, NY, pp 21–64

    Google Scholar 

  • 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

    Article  CAS  Google Scholar 

  • 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

    Article  CAS  Google Scholar 

  • 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

    Article  CAS  Google Scholar 

  • Kawai S, Ikeda S (1973) Studies on digestive enzymes of fishes. III. Development of digestive enzymes of rainbow trout after hatching and effect of dietary change on activities of digestive enzymes in the juvenile stage. Bull Jpn Soc Sci Fish 39:817–823

    Google Scholar 

  • Kohen R, Nyska A (2002) Invited review: oxidation of biological systems: oxidative stress phenomena, antioxidants, redox reactions, and methods for their quantification. Toxicol Pathol 30:620–650

    Article  CAS  PubMed  Google Scholar 

  • Kuz’mina VV (1996) Influence of age on digestive enzyme activity in some freshwater teleosts. Aquaculture 148:25–37

    Article  Google Scholar 

  • Lei XL, Chen R, Yang ZY (2003) Elementary study on nutritional compositions of the green alga, Ulva lactuca in the South China Sea. J Hainan Normal Univ 16(79–83):101

    Google Scholar 

  • Lovell RT (2002) Diet and fish husbandry. In: Halver JE, Hardy RW (eds) Fish Nutrition. Academic Press, San Diego, pp 703–754

    Google Scholar 

  • Mancini-Filho J, Novoa AV, Gonzalez AEB, Andrade-Wartha ERS, Silva AM, Pinto JR, Mancini DAP (2009) Free phenolic acids from the seaweed Halimeda monile with antioxidant effect protecting against liver injury. Z Naturforsch C 64:657–663

    Article  CAS  PubMed  Google Scholar 

  • Marinho G, Nunes C, Sousa-Pinto I, Pereira R, Rema P, Valente LMP (2013) The IMTA- cultivated Chlorophyta Ulva spp. as a sustainable ingredient in Nile tilapia (Oreochromis niloticus) diets. J Appl Phycol 25:1359–1367

    Article  CAS  Google Scholar 

  • Matanjun P, Mohamed S, Kharidah M, Noordin MM (2010) Comparison of cardiovascular protective effects of tropical seaweeds, Eucheuma cottonii, Caulerpa lentillifera, and Sargassum polycystum, on high-cholesterol/high-fat diet in rats. J Med Food 13:792–800

    Article  CAS  PubMed  Google Scholar 

  • Mohamed S, Hashim SN, Rahman HA (2012) Seaweeds: a sustainable functional food for complementary and alternative therapy. Trends Food Sci Technol 23:83–96

    Article  CAS  Google Scholar 

  • Morita K, Nakano T (2002) Seaweed accelerates the excretion of dioxin stored in rats. J Agric Food Chem 50:910–917

    Article  CAS  PubMed  Google Scholar 

  • Mustafa MG, Nakagawa H (1995) A review: dietary benefits of algae as an additive in fish feed. Isr J Aquacult 47:155–162

    Google Scholar 

  • Mustafa MG, Wakamatsu S, Takeda TA, Umino T, Nakagawa H (1995) Effects of algae meal as feed additive on growth, feed efficiency and body composition in red sea bream. Fish Sci 61:25–28

    CAS  Google Scholar 

  • Nakagawa H, Kasahara S, Sugiyama T (1987) Effect of Ulva meal supplementation on lipid metabolism of black sea bream, Acanthopagrus schlegeli. Aquaculture 62:109–121

    Article  Google Scholar 

  • 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

    Article  Google Scholar 

  • Nakano M (1990) Assay for superoxide dismutase based on chemiluminescence of luciferin analog. Methods Enzymol 186:227–232

    Article  CAS  PubMed  Google Scholar 

  • Nandeesha MC, Gangadhar B, Varghese TJ, Keshavanath P (1998) Effect of feeding Spirulina platensis on the growth, proximate composition and organoleptic quality of common carp, Cyprinus carpio L. Aquacult Res 29:305–312

    Article  Google Scholar 

  • Nielsen MM, Bruhn A, Rasmussen MB, Olesen B, Larsen MM, Møller HB (2012) Cultivation of Ulva lactuca with manure for simultaneous bioremediation and biomass production. J Appl Phycol 24:449–458

    Article  Google Scholar 

  • Pham MA, Lee KJ, Lee BJ, Lim SJ, Kim SS, Lee YD, Heo MS, Lee KW (2006) Effects of dietary Hizikia fusiformis on growth and immune responses in juvenile olive flounder (Paralichtys olivaceus). Asian-Aust J Anim Sci 19:1769–1775

    Article  CAS  Google Scholar 

  • Pyle GG, Kamunde CN, McDonald DG, Wood CM (2003) Dietary sodium inhibits aqueous copper uptake in rainbow trout (Oncorhynchus mykiss). J Exp Biol 206:609–618

    Article  CAS  PubMed  Google Scholar 

  • Rao JV (2006) Toxic effects of novel organophosphorus insecticide (RPR-V) on certain biochemical parameters of euryhaline fish, Oreochromis mossambicus. Pestic Biochem Physiol 86:78–84

    Article  CAS  Google Scholar 

  • Rausch PG, Moore TG (1975) Granule enzymes of polymorphonuclear neutrophils: A phylogenetic comparison. Blood 46:913–919

    CAS  PubMed  Google Scholar 

  • Reitman S, Frankel S (1957) A colorimetric method for the determination of serum glutamic oxalacetic and glutamic pyruvic transaminases. Am J Clin Pathol 28:53–56

    Article  Google Scholar 

  • Robaina L, Izquierdo MS, Moyano FJ, Socorro J, Vergara JM, Montero D, Fernández-Palacios H (1995) Soybean and lupin seed meals as protein sources in diets for gilthead seabream (Sparus aurata). Nutritional and histological implications. Aquaculture 130:219–233

    Article  Google Scholar 

  • Rupérez P, Saura-Calixto F (2001) Dietary fibre and physicochemical properties of edible Spanish seaweeds. Eur Food Res Technol 212:349–354

    Article  Google Scholar 

  • Sathivel A, Raghavendran RH, Srinivasan P, Devaki T (2008) Anti-peroxidative and anti-hyperlipidemic nature of Ulva lactuca crude polysaccharide on D-galactosamine induced hepatitis in rats. Food Chem Toxicol 46:3262–3267

    Article  CAS  PubMed  Google Scholar 

  • Satoh K, Nakagawa H, Kasahara S (1987) Effect of Ulva meal supplementation on disease resistance of red sea bream. Nippon Suisan Gakkaishi 53:1115–1120

    Article  Google Scholar 

  • 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 s19:233–271

    Google Scholar 

  • Sheikhzadeh N, Tayefi-Nasrabadi H, Oushani AK, Enferadi MHN (2012) Effects of Haematococcus pluvialis supplementation on antioxidant system and metabolism in rainbow trout (Oncorhynchus mykiss). Fish Physiol Biochem 38:413–419

    Article  CAS  PubMed  Google Scholar 

  • Silva DM, Valente LMP, Sousa-Pinto I, Pereira R, Pires MA, Seixas F, Rema P (2014) Evaluation of IMTA-produced seaweeds (Gracilaria, Porphyra, and Ulva) as dietary ingredients in Nile tilapia, Oreochromis niloticus L., juveniles. Effects on growth performance and gut histology. J Appl Phycol. doi:10.1007/s10811-014-0453-9:1-10

    Google Scholar 

  • Soler-Vila A, Coughlan S, Guiry MD, Kraan S (2009) The red alga Porphyra dioica as a fish feed ingredient for rainbow trout (Oncorhynchus mykiss): effects on growth, feed efficiency, and carcass composition. J Appl Phycol 21:617–624

    Article  Google Scholar 

  • Tacon AGJ, Hasan MR, Metian M (2011) FAO Fisheries and Aquaculture Technical Paper. 564

  • Tocher DR, Mourente G, Eecken AVD, Evjemo JO, Diaz E, Bell J, Geurden I, Lavens P, Olsen Y (2002) Effects of dietary vitamin E on antioxidant defence mechanisms of juvenile turbot (Scophthalmus maximus L.), halibut (Hippoglossus hippoglossus L.) and sea bream (Sparus aurata L.). Aquacult Nutr 8:195–207

    Article  CAS  Google Scholar 

  • 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

    Article  Google Scholar 

  • 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

    Article  CAS  Google Scholar 

  • 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. Aquacult Res 32:315–322

    Article  Google Scholar 

  • 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

    Article  Google Scholar 

  • Yone Y, Furuichi M, Urano K (1986) Effects of dietary wakame Undaria penatifida and Ascophyllum nodosum supplements on growth, feed efficiency, and proximate compositions of liver and muscle of red sea bream. Bull Jpn Soc Sci Fish 52:1465–1468

    Article  Google Scholar 

  • Zhang SJ (1996) The species and distribution of seaweeds in the coast of China seas. Chin Biodivers 4:139–144 (in Chinese with English abstract)

    Google Scholar 

Download references

Acknowledgments

This study was supported by grant no. 41276179 and no. 41276179 from the National Natural Science Foundation of China, grant no. S2011030005257 from the Guangdong Natural Science Foundation, and grant no. 2010B020201015 from the Guangdong Science and Technology Funding Scheme, and the authors thank Prof. Chiju Wei of the School of Sciences, Shantou University, China, for reviewing the manuscript and his helpful suggestions.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Xiaobo Wen.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Zhu, D., Wen, X., Xuan, X. et al. The green alga Ulva lactuca as a potential ingredient in diets for juvenile white spotted snapper Lutjanus stellatus Akazaki. J Appl Phycol 28, 703–711 (2016). https://doi.org/10.1007/s10811-015-0545-1

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10811-015-0545-1

Keywords

Navigation