Abstract
The fast growing of global aquaculture industry accompanied with increasing pressure on the supply and price of traditional feed materials (e.g., fish meal and soy bean meal). This circumstance has urged the need to search alternative sources of feed stuff. Food waste was used as feed stuff in rearing fish which possess substantial protein and lipid. Grass carp are major species reared in Hong Kong with lower nutritional requirements; it is also an ideal species for investigating the feasibility of using food waste as fish feeds for local aquaculture industry. The growth and immunity, reflected by total protein, total immunologlobulin (IgI), and nitroblue tetrazolium (NBT) activity of grass carp blood, were depressed when feeding with food waste feeds without enzymes. However, the supplementation of bromelain and papain in fish feed enhanced the efficient use of food waste by grass carp, which in turn improved the fish immunity. The present results indicated that the addition of those enzymes could enhance the feed utilization by fish and hematological parameters of grass carp, and the improvement on growth and immunity superior to the control (commercial feed) was observed with the addition of bromelain and papain supplement. Addition of 1 and 2 % mixture of bromelain and papain could significantly enhance the lipid utilization in grass carp.
Similar content being viewed by others
References
Alatise PS, Ogundele O, Eyo AA, Oludunjoye F (2006) Evaluation of different soybean-based diets on growth and nutrient utilization of Heterobranchus longifilis in aquaria tanks. FISON Conference Proceeding. pp 255-262
Ali A, Al-Asgah NA (2001) Effect of feeding different carbohydrate to lipid ratios on the growth performance and body composition of Nile Tilapia (Oreochromis niloticus) fingerlings. Anim Res 50:91–100
Anderson DP (1992) Immunostimulants, adjuvants, and vaccine carriers in fish: application to aquaculture. Annu Rev Fish Dis 2:281–307
Anderson DP, Siwicki AK (1995) Basic haematology and serology for fish health programs. In: Shariff M, Arthur JR, Subasinghe RP (eds) Diseases in Asian aquaculture II. Fish health section, Asian Fisheries Society, Manila, pp 185–202
AOAC (1984) Association of Official Analytical Chemists. Fibre (crude) in animal feed (962.06). In Official methods of analysis, Association of Official Analytical Chemists, 14th Edition. Washington, DC, pp 160–162
AOAC (1990a) Moisture in peat. (967.03) Official methods of analysis. 1990. Association of Official Analytical Chemists. 15th Edition
AOAC (1990b) Ash of animal feed. (942.05) Official methods of analysis. 1990. Association of Official Analytical Chemists, 15th Edition
Araba M, Dale NM (1990) Evaluation of KOH solubility as an indicator of overprocessing soybean meal. Poult Sci 69:76–83
Boonyaratpalin M, Promkunthong W, Hunter B (2000) Effects of enzyme pre-treatment on in vitro glucose solubility of Asian plant by-products and growth and digestibility of oil palm expeller meal by Oreochromis niloticus (Nile tilapia). Proceedings of the Third European Symposium on Feed Enzymes, TNO Voeding, The Netherlands pp 86-92
Bradford MM (1976) A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Anal Biochem 72:248–254
Castell JD, K Tiews (1980) Report on the EIFAC, IUNS and ICES working group on the standardization of methodology in fish nutrition research. Hamburg, Federal Republic of Germany, EIFAC Technical Paper
Chatzifotis S, Panagiotidou M, Papaioannou N, Pavlidis M, Nengas I, Mylonas CC (2010) Effect of dietary lipid levels on growth, feed utilization, body composition and serum metabolites of meagre (Argyrosomus regius) juveniles. Aquaculture 307:65–70
Deka A, Sahu NP, Jain KK (2003) Utilization of fruit processing wastes in the diet of Labeo rohita fingerling. Asian-Australas J Anim Sci 16:1661–1665
Du ZY, Tian LX, Liang GY, Liu YJ (2009) Effect of dietary energy to protein ratios on growth performance and feed efficiency of juvenile grass carp (Ctenopharyngodon idella). Open Fish Sci J 2:25–31
EPD (2012) Monitoring of solid waste in Hong Kong—waste statistics for 2011. Environmental Protection Department, Hong Kong SAR Government
EPD (2014) A food waste & yard waste plan for Hong Kong 2014–2022. Environmental Protection Department, Hong Kong SAR Government
Farhangi M, Carter CG (2007) Effect of enzyme supplementation to dehulled lupin-based diets on growth, feed efficiency, nutrient digestibility and carcass composition of rainbow trout, Oncorhynchus mykiss (Walbaum). Aquac Res 38:1274–1282
Fennema OR (1996) Food chemistry, 3rd edn. Marcel Decker, New York
Gauquelin F, Cuzona G, Gaxiolab G, Rosasb C, Arenab L, Bureauc DP, Cocharda JC (2007) Effect of dietary protein level on growth and energy utilization by Litopenaeus stylirostris under laboratory conditions. J Aquac 271:439–448
Goda AMA, Mabrouk HAH, Wafa MAE, El-Afifi TM (2012) Effect of using baker’s yeast and exogenous digestive enzymes as growth promoters on growth, feed utilization and hematological indices of Nile tilapia, Oreochromis niloticus fingerlings. J Agric Sci Technol B 2:15–28
Hasan MR, Hecht T, De Silva SS, Tacon AGJ (2007) Study and analysis of feeds and fertilizers for sustainable aquaculture development.FAO Fisheries Technical Paper No. 497. Rome, FAO. 510 pp
Helland SJ, Storebakken T, Grisdale-Helland B (1991) Atlantic salmon, Salmo salar. In: Wilson RP (ed) Handbook of nutrient requirement of finfish. CRC Press, Boca Raton, pp 13–22
Helmy AM, Badawi HK, Bishry AE (1974) Seasonal variations in the protein composition of blood serum of Anguilla vulgaris and Mugill cephalus. Egypt J Aquat Res 4:369–375
Jantrarotai W, Sitasit P, Jantrarotai P (1998) Protein and energy levels for maximum growth, diet utilization, yield of edible flesh and protein sparing of hybrid clarias catfish (Clarias macrocephalus x Clarias gariepinus). J World Aquacult Soc 29:281–289
Kang HY, Yang PY, Dominy WG, Lee CS (2010) Bioprocessing papaya processing waste for potential aquaculture feed supplement—economic and nutrient analysis with shrimp feeding trial. Bioresour Technol 101:7973–7979
Kolkovski S, Tandler A, Izquierdo MS (1997) Effects of live food and dietary digestive enzymes on the efficiency of microdiets for seabass (Dicentrarchus labrax) larvae. Aquaculture 148:313–322
Li SC, Takaoka O, Lee SW, Hwang JH, Kim YS, Ishimaru K, Seoka M, Jeong GS, Takii K (2009) Effect of dietary medicinal herbs on lipid metabolism and stress recovery in red sea bream Pagrus major. Fish Sci 75:665–672
Liebert F, Portz L (2005) Nutrient utilization of Nile Tilapia, Oreochromis niloticus fed plant based low phosphorus diets supplemented with graded levels of different sources of microbial phytase. Aquaculture 248:111–119
Lin D (1991) Grass carp, Ctenopharyngodon idella. In: Wilson RP (ed) Handbook of nutrient requirement of finfish. CRC Press, Boca Raton, pp 89–96
Lundstedt LM, Melo JFB, Santos-Neto C, Moraes G (2002) Diet influences proteolytic enzyme profile of the South American catfish Rhamdia quelen. Proceedings of International Congress on the Biology of Fish, Biochemistry and Physiology Advances in Finfish Aquaculture, Vancouver, Canada, pp. 65–71
Luo Z, Liu YJ, Mai KS, Tian LX, Liu DH, Tan XY (2004) Optimal dietary protein requirement of grouper Epinephelus coioides juveniles fed isoenergetic diets in floating net cages. Aquac Nutr 10:247–252
Luo Z, Liu YJ, Mai KS, Tian LX, Liu DH, Tan XY, Lin HZ (2005) Effect of dietary lipid level on growth performance, feed utilization and body composition of grouper Epinephelus coioides juveniles fed isonitrogenous diets in floating netcages. Aquac Int 13:257–269
McGoogan BB, Gatlin DM (2000) Dietary manipulations affecting growth and nitrogenous waste production of red drum, Sciaenops ocellatus. Aquaculture 209:209–218
Metherel AH, Taha AY, Izadi H, Stark KD (2009) The application of ultrasound energy to increase lipid extraction throughput of solid matrix samples (flaxseed). Prostaglandins Leukot Essent Fatty Acids 81:417–423
Meyer G, Fracalossi DM (2004) Protein requirement of jundia fingerlings, Rhamdia quelen, at two dietary energy concentrations. Aquaculture 240:331–343
Miyamoto D, Watanabe J, Ishihara K (2004) Effect of water-soluble phospholipids polymers conjugated with papain on the enzymatic stability. Biomaterials 25:71–76
NRC (1993) Nutrient Requirements of Fish. National Research Council. Washington, DC, USA, National Academic Press, Washington, DC, USA
Osman HAM, Ibrahim TB, Soliman WE, Monier MM (2010) Influence of dietary commercial Beaker’s yeast, Saccharomyces cerevisae on growth performance, survival and immunostimulation of Oreochromis niloticus challenged with Aeromonas hydrophila. Nat Sci 8:96–103
Sahu S, Das BK, Mishra BK, Pradhan J, Sarangi N (2007) Effect of Allium sativum on the immunity of Labeo rohita infected with Aeromonas hydrophila. J Appl Ichthyol 23:80–86
Singh P, Maqsood S, Samoon MH, Phulia V, Danish M, Chalal RS (2011) Exogenous supplementation of papain as growth promoter in diet of fingerlings of Cyprinus carpio. Int Aquat Res 3:1–9
Siwicki AK, Anderson DP, Rumsey GL (1994) Dietary intake of immunostimulants by rainbow trout affects non-specific immunity and protection against furunculosis. Vet Immunol Immunopathol 41:125–139
Wiegertjes GF, Stet RJM, Parmentier HK, Vas Muiswinkel WB (1996) Immunogenetics of disease resistance in fish: a comparable approach. Dev Comp Immunol 20:365–381
Wilson RP, Halver RP (1986) Protein and amino acid requirements of fishes. Annu Rev Nutr 6:225–244
Wong MH, Tang LY, Kwok FSL (1996) The use of enzyme digested soybean residue for feeding common carp. Biomed Environ Sci 9:418–442
Wu W, Hettiarachchy NS, Qi M (1998) Hydrophobicity, solubility, and emulsifying properties of soy protein peptides prepared by papain modification and ultrafiltration. J Am Oil Chem Soc 75:845–850
Wu XY, Liu YJ, Tian LX, Mai KS, Yang HJ, Liang GY (2007) Effects of raw corn starch levels on growth, feed utilization, plasma chemical indices and enzyme activities in juvenile yellowfin seabream Sparus latus Houttuyn. Aquac Res 38:1330–1338
Yousefian M, Navazandeh A, Gharaati A, Mahdavi S (2013) Investigation of survival, growth and biochemical blood parameters of common carp (Cyprinus carpio L.) larvae feed by artificial diets. Int J Plant Anim Environ Sci 3:175–180
Acknowledgments
Financial support from Environment and Conservation Fund (37/2009) of the Hong Kong SAR Government is gratefully acknowledged.
Author information
Authors and Affiliations
Corresponding author
Additional information
Responsible editor: Philippe Garrigues
Rights and permissions
About this article
Cite this article
Choi, W.M., Lam, C.L., Mo, W.Y. et al. Upgrading food wastes by means of bromelain and papain to enhance growth and immunity of grass carp (Ctenopharyngodon idella). Environ Sci Pollut Res 23, 7186–7194 (2016). https://doi.org/10.1007/s11356-015-4863-2
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s11356-015-4863-2