Research Article
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Year 2020, Volume: 3 Issue: 1, 24 - 35, 01.01.2020

Cayen Sédro Alofa , Alphonse Adıte , Youssouf Abou

https://doi.org/10.3153/AR20003

Abstract

References

  • Abdelkhalek, N.K.M., Ghazy, EW., Abdel-Daim M.M. (2015). Pharmacodynamic interaction of Spirulina platensis and deltamethrin in freshwater fish Nile tilapia, Oreochromis niloticus: impact on lipid peroxidation and oxidative stress. Environmental Science and Pollution Research, 22(4), 3023-3031. https://doi.org/10.1007/s11356-014-3578-0
  • Abou, Y., Fiogbé, E.D., Micha, J.C. (2007a). A preliminary assessment of growth and production of Nile tilapia, Oreochromis niloticus L., fed azolla-based-diets in earthen ponds. Journal of Applied Aquaculture, 19(4), 55-69. https://doi.org/10.1300/J028v19n04_03
  • Abou, Y., Fiogbé E.D., Micha, J.C. (2007b). Effects of stocking density on growth, yield and profitability of farming Nile tilapia, Oreochromis niloticus L., fed Azolla diet, in earthen ponds. Aquaculture Research, 38(6), 595-604. https://doi.org/10.1111/j.1365-2109.2007.01700.x
  • Adler, S., Honkapää, K., Saarela, M., Slizyte, R., Sterten, H., Vikman, M., Løes, A.K. (2014). Utilisation of co-streams in the Norwegian food processing industry: A multiple case study. Bioforsk Report, 9(82), 1-58.
  • Ahmad Dar, B., Khaliq, R., Jha, G.N., Kour, P., Qureshi, T.A. (2014). Protective effects of dietary spirulina against cadmium chloride exposed histoarchitectural changes in the liver of freshwater catfish Clarias batrachus (Linnaeus, 1758). Indian Journal of Fisheries, 61(3), 83-87.
  • Al-Feky, S.S.A., El-Sayed, A.F.M., Ezzat, A.A. (2016). Dietary taurine enhances growth and feed utilization in larval Nile tilapia (Oreochromis niloticus) fed soybean meal-based diets. Aquaculture Nutrition, 22(2), 457-464. https://doi.org/10.1111/anu.12266
  • Alofa, C.S., Oke, V., Abou, Y. (2016). Effect of replacement of fish meal with broiler chicken viscera on growth, feed utilization and production of African catfish Clarias gariepinus (Burchell, 1822). International Journal of Fisheries and Aquatic Studies, 4(6), 182-186.
  • Beresto, V. (2001). Our experience in spirulina feeding to minks in the reproduction period. Scientifur, 25(1), 11-15.
  • Bhujel, R.C. (2000). A rewiew of strategies for the management of Nile tilapia (Oreochromis niloticus) broodfish in seed production systems, especially hapa-based systems. Aquaculture, 181(1-2), 37-59. https://doi.org/10.1016/S0044-8486(99)00217-3
  • Biswas, A., Araki, H., Sakata, T., Nakamori, T., Kato, K., Takii, K. (2017). Fish meal replacement by soy protein from soymilk in the diets of red sea bream (Pagrus major). Aquaculture Nutrition, 23(6), 1379-1389. https://doi.org/10.1111/anu.12513
  • Cho, J.H., Kim, I.H. (2011). Fish meal nutritive value. Journal of Animal Physiology and Animal Nutrition, 95(6), 685-692. https://doi.org/10.1111/j.1439-0396.2010.01109.x
  • Dagnelie, L. (1975). Théories et méthodes statistiques. Presses Agronomiques de Gembloux, Belgique, 463p. ISBN-10: 2870160070.
  • Emeka, A.I., Oscar, E.V. (2016). Comparative Study of Growth Performance, Food Utilization and Survival of the African Catfish Clarias gariepinus (Burchell, 1822) Fingerlings Fed Live Maggot (Musca domestica) and Coppens Commercial Feed. International Journal of Scientific Research in Science, Engineering and Technology, 2(2), 379-386.
  • Esmaeili, M., Abedian Kenari, A., Rombenso, A.N. (2017). Effects of fish meal replacement with meat and bone meal using garlic (Allium sativum) powder on growth, feeding, digestive enzymes and apparent digestibility of nutrients and fatty acids in juvenile rainbow trout (Oncorhynchus mykiss Walbaum, 1792). Aquaculture Nutrition, 23(6), 1225-1234. https://doi.org/10.1111/anu.12491
  • FAO, (2016). The state of world fisheries and aquaculture 2016. Contributing to food security and nutrition for all. Food and Agriculture Organization of the United Nations (FAO), Rome. ISBN 978-92-5-209185-1
  • Folch, J., Lees M., Sloane-Stanley, G.H. (1957). A simple method for the isolation and purification of total lipids from animal tissues. Journal of Biological Chemistry, 226, 497-509.
  • Guimarães, I.G., Pezzato, L.E., Barros, M.M., Tachibana, L. (2008). Nutrient digestibility of cereal grain products and by-products in extruded diets for Nile tilapia. Journal of The World Aquaculture Society, 39(6), 781-789. https://doi.org/10.1111/j.1749-7345.2008.00214.x
  • Güroy, B., Sahin, I., Mantoglu, S., Kayalı, S. (2012). Spirulina as a natural carotenoid source on growth, pigmentation and reproductive performance of yellowtail cichlid Pseudotropheus acei. Aquaculture International, 20(5), 869-878. https://doi.org/10.1007/s10499-012-9512-x
  • Hemaiswarya, S., Raja, R., Ravi-Kumar, R., Ganesan, V., Anbazhagan, C. (2011). Microalgae: a sustainable feed source for aquaculture. World Journal of Microbiology and Biotechnology, 27(8), 1737-1746. https://doi.org/10.1007/s11274-010-0632-z
  • Herath, S.S., Haga, Y., Satoh, S. (2016). Potential use of corn co products in fishmeal free diets for juvenile Nile tilapia Oreochromis niloticus. Fisheries Science, 82(5), 811-818. https://doi.org/10.1007/s12562-016-1008-6
  • Horwitz, W., Latimer, GW. (2005). Official Methods of Analysis of AOAC International. 18th Edition, Association of Official Analytical Chemistry International, Maryland ISBN: 0935584757 9780935584752 093558482X 9780935584820
  • Huo S., Wang, Z., Zhu, S., Zhou, W., Dong, R., Yuan, Z. (2012). Cultivation of Chlorella zofingiensis in bench-scale outdoor ponds by regulation of pH using dairy wastewater in winter, South China. Bioresource Technology, 121, 76-82. https://doi.org/10.1016/j.biortech.2012.07.012
  • James, R., Sampath, K., Thangarathinam, R., Vasudevan, I. (2006). Effect of dietary spirulina level on growth, fertility, coloration and leucocyte count in red swordtail, Xiphophorus helleri. Israeli Journal of Aquaculture - Bamidgeh, 58(8), 97-104.
  • Kader, M.A., Bulbul, M., Koshio, S., Ishikawa, M., Yokoyama, S., Nguyen, B.T., Komilus, C.F. (2012). Effect of complete replacement of fish meal by dehulled soybean meal with crude attractants supplementation in diets for red sea bream, Pagrus major. Aquaculture, 350-353, 109-116. https://doi.org/10.1016/j.aquaculture.2012.04.009
  • Kader, M.A., Koshio, S. (2012). Effect of composite mixture of seafood by-products and soybean proteins in replacement of fishmeal on the performance of red sea bream, Pagrus major. Aquaculture, 368, 95-102. https://doi.org/10.1016/j.aquaculture.2012.09.014
  • Krome, C., Jauncey, K., Focken, U. (2016). Jatropha curcas kernel meal as a replacement for fishmeal in practical Nile tilapia, Oreochromis niloticus feeds. AACL Bioflux, 9(3), 590-596.
  • Le Vay, L., Jones, D., Puello-Cruz, A., Sangha R., Ngamphonsai, C. (2001). Digestion in relation to feeding strategies exhibited by crustacean larvae. Comparative Biochemistry and Physiology Part A: Molecular & Integrative Physiology, 128(3), 623-630. https://doi.org/10.1016/S1095-6433(00)00339-1
  • Lin Y.H., Mui J.J. (2016). Evaluation of dietary inclusion of housefly maggot (Musca domestica) meal on growth, fillet composition and physiological responses for barramundi, Lates calcarifer. Aquaculture Research, 48, 2478-2485. https://doi.org/10.1111/are.13085
  • Newton, L., Sheppard, C., Watson, D.W., Burtle, G., Dove, R. (2005). Using the black soldier fly, Hermetia illucens, as a value-added tool for the management of swine manure. Anim. Poult. Waste Manag. Center, North Carolina, State Univ. Raleigh, NC 19p.
  • Ogunji, J.O., Kloas, W., Wirth, M., Schulz, C., Rennert, B. (2008). Housefly maggot meal (magmeal) as a protein source for Oreochromis niloticus (Linn.). Asian Fisheries Science, 21, 319-331.
  • Oyelese, O.A. (2007). Utilization of compounded ration and maggot in the diet of Clarias gariepinus. Research Journal of Applied Sciences, 2(3), 301-306.
  • Palmegiano, G.B., Agradi, E., Forneris, G., Gai, F., Gasco, L., Rigamonti, E., Sicuro, B., Zoccarato, I. (2005). Spirulina as a nutrient source in diets for growing sturgeon (Acipenser baeri). Aquaculture Research, 36, 188-195. https://doi.org/10.1111/j.1365-2109.2005.01209.x
  • Promya, J., Chitmanat, C. (2011). The effects of Spirulina platensis and Cladophora algae on the growth performance, meat quality and immunity stimulating capacity of the African sharptooth catfish (Clarias gariepinus). International Journal of Agriculture and Biology, 13, 77-82.
  • Ramakrishnan, C.M., Haniffa, M.A., Manohar, M., Dhanaraj, M., Jesu Arockiaraj, A., Seetharaman, S., Arunsingh, S.V. (2008). Effects of probiotics and spirulina on survival and growth of juvenile common carp (Cyprinus carpio). The Israeli Journal of Aquaculture - Bamidgeh, 60(2), 128-133.
  • Salomone, R., Saija, G., Mondello, G., Giannetto, A., Fasulo, S., Savastano, D. (2017). Environmental impact of food waste bioconversion by insects: application of life cycle assessment to process using Hermetia illucens. Journal of Cleaner Production, 140(2), 890-905. https://doi.org/10.1016/j.jclepro.2016.06.154
  • Sealey, W.M., Gaylord T.G., Barrows F.T., Tomberlin J.K., McGuire M.A., Ross C., St-Hilaire S. (2011). Sensory analysis of rainbow trout, Oncorhynchus mykiss, fed enriched black soldier fly prepupae, Hermetia illucens. Journal of the World Aquaculture Society, 42(1), 34-45. https://doi.org/10.1111/j.1749-7345.2010.00441.x
  • Silva-Neto, J.F., Nunes, A.J.P., Sabry-Neto, H., Sa, M.V.C. (2012). Spirulina meal has acted as a strong feeding attractant for Litopenaeus vannamei at a very low dietary inclusion level. Aquaculture Research, 43, 430-437. https://doi.org/10.1111/j.1365-2109.2011.02846.x
  • Sirakov, I., Velichkova, K., Nikolov, G. (2012). The effect of algae meal (Spirulina) on the growth performance and carcass parameters of rainbow trout (Oncorhynchus mykiss) J. Journal of Bioscience and Biotechnology, Special Edition, 151-156.
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Evaluation of Spirulina (Spirulina platensis) wastes and live housefly (Musca domestica) larvae as dietary protein sources in diets of Oreochromis niloticus (Linnaeus 1758) fingerlings

Year 2020, Volume: 3 Issue: 1, 24 - 35, 01.01.2020

Cayen Sédro Alofa , Alphonse Adıte , Youssouf Abou

https://doi.org/10.3153/AR20003

Abstract

This study was designed to evaluate spirulina
wastes and live housefly maggot as partial replacement for fishmeal in the
diets of Nile Tilapia. Four isonitrogenous (35%) and isocaloric (17-18 KJ.g-1)
diets were evaluated: commercial diet Skretting SK, control diet CD (30% fishmeal),
and two others diets (SW and LM), corresponding to spirulina wastes and live
housefly maggot inclusion
respectively. Diets were hand-fed thrice daily to triplicate groups of
fish to apparent satiation. After 12 weeks, the final weight and feed intake of
fish fed diet CD and SK did not differ from those fed diets LM, but were higher
than those fed SW diet (p<0.05).
However, inclusion of SW had no effect on feed utilization. No significant
differences were found in survival, feed conversion ratio, protein efficiency
ratio and condition factor among the treatments (p>0.05). Whole-body protein contents were similar in all groups,
whereas the lipid content was lower in SW group. It was concluded that a 62.56
% fishmeal protein could be replaced by live maggot in the diet of Nile Tilapia without negative effects on growth performances and quality of fish
produced.   

Keywords

Spirulina wastes Live maggots Fishmeal Growth Nile tilapia

Supporting Institution

Ministry of Higher Education and Scientific Research, Benin

Thanks

We are grateful to Mr. Appolinaire Effio, technician at the laboratory of zootechnics, Faculty of Agricultural Sciences, University of Abomey-Calavi for his assistance during the biochemical analysis. Mr Roger K. ADOUNKPE, Head of the Spirulina Production Unit of the Regional Center for Development and Health (Pahou, Benin) for the supply of spirulina by-products.

References

  • Abdelkhalek, N.K.M., Ghazy, EW., Abdel-Daim M.M. (2015). Pharmacodynamic interaction of Spirulina platensis and deltamethrin in freshwater fish Nile tilapia, Oreochromis niloticus: impact on lipid peroxidation and oxidative stress. Environmental Science and Pollution Research, 22(4), 3023-3031. https://doi.org/10.1007/s11356-014-3578-0
  • Abou, Y., Fiogbé, E.D., Micha, J.C. (2007a). A preliminary assessment of growth and production of Nile tilapia, Oreochromis niloticus L., fed azolla-based-diets in earthen ponds. Journal of Applied Aquaculture, 19(4), 55-69. https://doi.org/10.1300/J028v19n04_03
  • Abou, Y., Fiogbé E.D., Micha, J.C. (2007b). Effects of stocking density on growth, yield and profitability of farming Nile tilapia, Oreochromis niloticus L., fed Azolla diet, in earthen ponds. Aquaculture Research, 38(6), 595-604. https://doi.org/10.1111/j.1365-2109.2007.01700.x
  • Adler, S., Honkapää, K., Saarela, M., Slizyte, R., Sterten, H., Vikman, M., Løes, A.K. (2014). Utilisation of co-streams in the Norwegian food processing industry: A multiple case study. Bioforsk Report, 9(82), 1-58.
  • Ahmad Dar, B., Khaliq, R., Jha, G.N., Kour, P., Qureshi, T.A. (2014). Protective effects of dietary spirulina against cadmium chloride exposed histoarchitectural changes in the liver of freshwater catfish Clarias batrachus (Linnaeus, 1758). Indian Journal of Fisheries, 61(3), 83-87.
  • Al-Feky, S.S.A., El-Sayed, A.F.M., Ezzat, A.A. (2016). Dietary taurine enhances growth and feed utilization in larval Nile tilapia (Oreochromis niloticus) fed soybean meal-based diets. Aquaculture Nutrition, 22(2), 457-464. https://doi.org/10.1111/anu.12266
  • Alofa, C.S., Oke, V., Abou, Y. (2016). Effect of replacement of fish meal with broiler chicken viscera on growth, feed utilization and production of African catfish Clarias gariepinus (Burchell, 1822). International Journal of Fisheries and Aquatic Studies, 4(6), 182-186.
  • Beresto, V. (2001). Our experience in spirulina feeding to minks in the reproduction period. Scientifur, 25(1), 11-15.
  • Bhujel, R.C. (2000). A rewiew of strategies for the management of Nile tilapia (Oreochromis niloticus) broodfish in seed production systems, especially hapa-based systems. Aquaculture, 181(1-2), 37-59. https://doi.org/10.1016/S0044-8486(99)00217-3
  • Biswas, A., Araki, H., Sakata, T., Nakamori, T., Kato, K., Takii, K. (2017). Fish meal replacement by soy protein from soymilk in the diets of red sea bream (Pagrus major). Aquaculture Nutrition, 23(6), 1379-1389. https://doi.org/10.1111/anu.12513
  • Cho, J.H., Kim, I.H. (2011). Fish meal nutritive value. Journal of Animal Physiology and Animal Nutrition, 95(6), 685-692. https://doi.org/10.1111/j.1439-0396.2010.01109.x
  • Dagnelie, L. (1975). Théories et méthodes statistiques. Presses Agronomiques de Gembloux, Belgique, 463p. ISBN-10: 2870160070.
  • Emeka, A.I., Oscar, E.V. (2016). Comparative Study of Growth Performance, Food Utilization and Survival of the African Catfish Clarias gariepinus (Burchell, 1822) Fingerlings Fed Live Maggot (Musca domestica) and Coppens Commercial Feed. International Journal of Scientific Research in Science, Engineering and Technology, 2(2), 379-386.
  • Esmaeili, M., Abedian Kenari, A., Rombenso, A.N. (2017). Effects of fish meal replacement with meat and bone meal using garlic (Allium sativum) powder on growth, feeding, digestive enzymes and apparent digestibility of nutrients and fatty acids in juvenile rainbow trout (Oncorhynchus mykiss Walbaum, 1792). Aquaculture Nutrition, 23(6), 1225-1234. https://doi.org/10.1111/anu.12491
  • FAO, (2016). The state of world fisheries and aquaculture 2016. Contributing to food security and nutrition for all. Food and Agriculture Organization of the United Nations (FAO), Rome. ISBN 978-92-5-209185-1
  • Folch, J., Lees M., Sloane-Stanley, G.H. (1957). A simple method for the isolation and purification of total lipids from animal tissues. Journal of Biological Chemistry, 226, 497-509.
  • Guimarães, I.G., Pezzato, L.E., Barros, M.M., Tachibana, L. (2008). Nutrient digestibility of cereal grain products and by-products in extruded diets for Nile tilapia. Journal of The World Aquaculture Society, 39(6), 781-789. https://doi.org/10.1111/j.1749-7345.2008.00214.x
  • Güroy, B., Sahin, I., Mantoglu, S., Kayalı, S. (2012). Spirulina as a natural carotenoid source on growth, pigmentation and reproductive performance of yellowtail cichlid Pseudotropheus acei. Aquaculture International, 20(5), 869-878. https://doi.org/10.1007/s10499-012-9512-x
  • Hemaiswarya, S., Raja, R., Ravi-Kumar, R., Ganesan, V., Anbazhagan, C. (2011). Microalgae: a sustainable feed source for aquaculture. World Journal of Microbiology and Biotechnology, 27(8), 1737-1746. https://doi.org/10.1007/s11274-010-0632-z
  • Herath, S.S., Haga, Y., Satoh, S. (2016). Potential use of corn co products in fishmeal free diets for juvenile Nile tilapia Oreochromis niloticus. Fisheries Science, 82(5), 811-818. https://doi.org/10.1007/s12562-016-1008-6
  • Horwitz, W., Latimer, GW. (2005). Official Methods of Analysis of AOAC International. 18th Edition, Association of Official Analytical Chemistry International, Maryland ISBN: 0935584757 9780935584752 093558482X 9780935584820
  • Huo S., Wang, Z., Zhu, S., Zhou, W., Dong, R., Yuan, Z. (2012). Cultivation of Chlorella zofingiensis in bench-scale outdoor ponds by regulation of pH using dairy wastewater in winter, South China. Bioresource Technology, 121, 76-82. https://doi.org/10.1016/j.biortech.2012.07.012
  • James, R., Sampath, K., Thangarathinam, R., Vasudevan, I. (2006). Effect of dietary spirulina level on growth, fertility, coloration and leucocyte count in red swordtail, Xiphophorus helleri. Israeli Journal of Aquaculture - Bamidgeh, 58(8), 97-104.
  • Kader, M.A., Bulbul, M., Koshio, S., Ishikawa, M., Yokoyama, S., Nguyen, B.T., Komilus, C.F. (2012). Effect of complete replacement of fish meal by dehulled soybean meal with crude attractants supplementation in diets for red sea bream, Pagrus major. Aquaculture, 350-353, 109-116. https://doi.org/10.1016/j.aquaculture.2012.04.009
  • Kader, M.A., Koshio, S. (2012). Effect of composite mixture of seafood by-products and soybean proteins in replacement of fishmeal on the performance of red sea bream, Pagrus major. Aquaculture, 368, 95-102. https://doi.org/10.1016/j.aquaculture.2012.09.014
  • Krome, C., Jauncey, K., Focken, U. (2016). Jatropha curcas kernel meal as a replacement for fishmeal in practical Nile tilapia, Oreochromis niloticus feeds. AACL Bioflux, 9(3), 590-596.
  • Le Vay, L., Jones, D., Puello-Cruz, A., Sangha R., Ngamphonsai, C. (2001). Digestion in relation to feeding strategies exhibited by crustacean larvae. Comparative Biochemistry and Physiology Part A: Molecular & Integrative Physiology, 128(3), 623-630. https://doi.org/10.1016/S1095-6433(00)00339-1
  • Lin Y.H., Mui J.J. (2016). Evaluation of dietary inclusion of housefly maggot (Musca domestica) meal on growth, fillet composition and physiological responses for barramundi, Lates calcarifer. Aquaculture Research, 48, 2478-2485. https://doi.org/10.1111/are.13085
  • Newton, L., Sheppard, C., Watson, D.W., Burtle, G., Dove, R. (2005). Using the black soldier fly, Hermetia illucens, as a value-added tool for the management of swine manure. Anim. Poult. Waste Manag. Center, North Carolina, State Univ. Raleigh, NC 19p.
  • Ogunji, J.O., Kloas, W., Wirth, M., Schulz, C., Rennert, B. (2008). Housefly maggot meal (magmeal) as a protein source for Oreochromis niloticus (Linn.). Asian Fisheries Science, 21, 319-331.
  • Oyelese, O.A. (2007). Utilization of compounded ration and maggot in the diet of Clarias gariepinus. Research Journal of Applied Sciences, 2(3), 301-306.
  • Palmegiano, G.B., Agradi, E., Forneris, G., Gai, F., Gasco, L., Rigamonti, E., Sicuro, B., Zoccarato, I. (2005). Spirulina as a nutrient source in diets for growing sturgeon (Acipenser baeri). Aquaculture Research, 36, 188-195. https://doi.org/10.1111/j.1365-2109.2005.01209.x
  • Promya, J., Chitmanat, C. (2011). The effects of Spirulina platensis and Cladophora algae on the growth performance, meat quality and immunity stimulating capacity of the African sharptooth catfish (Clarias gariepinus). International Journal of Agriculture and Biology, 13, 77-82.
  • Ramakrishnan, C.M., Haniffa, M.A., Manohar, M., Dhanaraj, M., Jesu Arockiaraj, A., Seetharaman, S., Arunsingh, S.V. (2008). Effects of probiotics and spirulina on survival and growth of juvenile common carp (Cyprinus carpio). The Israeli Journal of Aquaculture - Bamidgeh, 60(2), 128-133.
  • Salomone, R., Saija, G., Mondello, G., Giannetto, A., Fasulo, S., Savastano, D. (2017). Environmental impact of food waste bioconversion by insects: application of life cycle assessment to process using Hermetia illucens. Journal of Cleaner Production, 140(2), 890-905. https://doi.org/10.1016/j.jclepro.2016.06.154
  • Sealey, W.M., Gaylord T.G., Barrows F.T., Tomberlin J.K., McGuire M.A., Ross C., St-Hilaire S. (2011). Sensory analysis of rainbow trout, Oncorhynchus mykiss, fed enriched black soldier fly prepupae, Hermetia illucens. Journal of the World Aquaculture Society, 42(1), 34-45. https://doi.org/10.1111/j.1749-7345.2010.00441.x
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  • Sirakov, I., Velichkova, K., Nikolov, G. (2012). The effect of algae meal (Spirulina) on the growth performance and carcass parameters of rainbow trout (Oncorhynchus mykiss) J. Journal of Bioscience and Biotechnology, Special Edition, 151-156.
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There are 47 citations in total.

Details

Primary Language English
Subjects Hydrobiology
Journal Section Research Articles
Authors

Cayen Sédro Alofa 0000-0002-3412-3362

Alphonse Adıte 0000-0002-2255-4464

Youssouf Abou 0000-0002-8273-0036

Publication Date January 1, 2020
Submission Date October 25, 2019
Published in Issue Year 2020Volume: 3 Issue: 1

Cite

APA Alofa, C. S., Adıte, A., & Abou, Y. (2020). Evaluation of Spirulina (Spirulina platensis) wastes and live housefly (Musca domestica) larvae as dietary protein sources in diets of Oreochromis niloticus (Linnaeus 1758) fingerlings. Aquatic Research, 3(1), 24-35. https://doi.org/10.3153/AR20003
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