Sains Malaysiana 53(3)(2024): 501-518

http://doi.org/10.17576/jsm-2024-5303-03

Hermetia illucens Larvae Meal as Partial Fishmeal Replacement in Jade Perch Diet Cultured in Biofloc: Growth Performance, Feed Efficiency and Consumer Acceptance

(Tepung Larva Hermetia illucens sebagai Pengganti Separa Tepung Ikan dalam Diet Jade Perch yang Dikultur dalam Bioflok: Prestasi Pertumbuhan, Kecekapan Makanan dan Penerimaan Pengguna)

NORHAYATI ZAINORAHIM¹, NORHIDAYAH MOHD TAUFEK^1,5,*, POO BALAN GANESAN^3,6, GEOK YUAN ANNIE TAN²  & HANAN MOHD YUSOF⁴

¹Aqua-Nutri Biotech Research Laboratory, Institute of Biological Sciences, Faculty of Science, Universiti Malaya, 50603 Kuala Lumpur, Malaysia

²Institute of Biological Sciences, Faculty of Science, Universiti Malaya, 50603 Kuala Lumpur, Malaysia

³Department of Mechanical Engineering, Faculty of Engineering, Universiti Malaya, 50603 Kuala Lumpur, Malaysia

⁴Fisheries Research Institute (FRI), Glami Lemi, Department of Fisheries, Titi, 71650 Jelebu, Negeri Sembilan, Malaysia

⁵Ladang Mini, Institute of Biological Sciences, Faculty of Science, Universiti Malaya, 50603 Kuala Lumpur, Malaysia

⁶Centre for Research in Biotechnology for Agriculture (CEBAR), Level 3, Research Management & Innovation Complex, Universiti Malaya, 50603 Kuala Lumpur, Malaysia

Diserahkan: 8 Jun 2023/Diterima: 16 Februari2024

Abstract

A 12-week feeding trial on jade perch (Scortum barcoo) was conducted to evaluate the outcomes of partial substitution of fishmeal with black soldier fly larvae meal (BSFLM) in a biofloc system that requires minimal water exchange. The jade perch juveniles were subjected to three dietary treatments namely the 100% fishmeal (FM100), 50% BSFLM (BSF50), and a commercial diet (COM) with 20 individuals per treatment in triplicate tanks. Growth, feed efficiency, and body indices were measured throughout the feeding trial. There were no significant differences observed between the treatments in growth indicators such as the body weight gain (84.55 - 89.10 g), feed conversion ratio (1.77 - 1.87), specific growth rate (1.71 - 1.81 %/day), protein efficiency ratio (1.69 - 1.77), survival rate (90.00 - 98.48 %) and fillet yield (34.94 - 37.08 %). The condition factor is similar in all treatment groups ranging from 1.97 - 2.05. The crude protein and moisture content making up fish body composition are not statistically different among treatments, but higher crude lipids are obtained in the BSF50 (32.33 ± 5.27 g/kg) and COM (31.67 ± 2.76 g/kg). Higher hepatosomatic index (HSI) and visceral fat somatic index (VFSI) values were observed in BSF50 group at 3.13 ± 0.25 and 10.89 ± 1.68, respectively. Furthermore, sensory evaluation comparing the consumers' evaluation and acceptance of the fish cultured with the different dietary treatment and culture system shows that the group fed BSF50 and cultured in biofloc system received similar overall appreciation with the FM100 and COM group. In conclusion, BSFLM inclusion in the jade perch diet, combined with the biofloc system, is feasible to be explored further.

Keywords: Alternative feed; aquatic animals; biofloc technology; insect protein; sustainable aquaculture

Abstrak

Suatu kajian pemakanan selama 12 minggu ke atas ikan jade perch (Scortum barcoo) telah dijalankan untuk menilai hasil daripada penggantian separa tepung ikan dengan tepung larva lalat askar hitam (BSFLM) dalam sistem bioflok yang memerlukan pertukaran air yang minimum. Juvenil ikan jade perch telah diberikan tiga rawatan pemakanan iaitu 100% tepung ikan (FM100), 50% BSFLM (BSF50) dan diet komersial (COM) dengan 20 ekor individu untuk setiap rawatan dalam tiga kali pengulangan tangki. Pertumbuhan, kecekapan pemakanan, dan indeks badan telah diukur sepanjang ujian pemakanan. Tiada perbezaan yang signifikan diperhatikan antara rawatan tersebut dalam indikator pertumbuhan seperti pertambahan berat badan (84.55 - 89.10), nisbah penukaran makanan (1.77 - 1.87), kadar pertumbuhan khusus (1.71 - 1.81 %/day), nisbah kecekapan protein (1.69 - 1.77), kadar kemandirian (90.00 - 98.48%) dan hasil filet (34.94 - 37.08%). Faktor keadaan adalah serupa dalam semua kumpulan rawatan dengan julat 1.97 - 2.05. Kandungan protein kasar dan lembapan yang membentuk komposisi badan ikan tidak berbeza secara statistik antara rawatan, tetapi lemak kasar yang lebih tinggi diperoleh dalam BSF50 (32.33 ± 5.27 g/kg) dan COM (31.67 ± 2.76 g/kg). Nilai indeks hepatosomatik (HSI) dan indeks somatik lemak viseral (VFSI) yang lebih tinggi telah diperhatikan dalam kumpulan BSF50 masing – masing pada 3.13 ± 0.25 dan 10.89 ± 1.68. Selain itu, penilaian deria yang membandingkan penilaian dan penerimaan pengguna terhadap ikan yang dibiakkan dengan rawatan pemakanan dan sistem penternakan yang berbeza menunjukkan bahawa kumpulan yang diberi BSF50 dan dibiakkan dalam sistem bioflok menerima penghargaan keseluruhan yang serupa dengan kumpulan FM100 dan COM. Kesimpulannya, penggunaan BSFLM dalam diet jade perch, yang digabungkan dengan sistem bioflok, adalah wajar untuk dikaji lebih lanjut.

Kata kunci: Akuakultur mampan; haiwan akuatik; makanan alternatif; protein serangga; teknologi bioflok

RUJUKAN

Abakari, G., Luo, G. & Kombat, E.O. 2021. Dynamics of nitrogenous compounds and their control in biofloc technology (BFT) systems: A review. Aquaculture and Fisheries 6(5): 441-447.

Abdel-Tawwab, M., Khalil, R.H., Metwally, A.A., Shakweer, M.S., Khallaf, M.A. & Abdel-Latif, H.M.R. 2020. Effects of black soldier fly (Hermetia illucens L.) larvae meal on growth performance, organs-somatic indices, body composition, and hemato-biochemical variables of European sea bass, Dicentrarchus labrax. Aquaculture 522: 735136.

Abu Bakar, N.S., Mohd Nasir, N., Lananan, F., Abdul Hamid, S.H., Lam, S.S. & Jusoh, A.  2015. Optimization of C/N ratios for nutrient removal in aquaculture system culturing African catfish, (Clarias gariepinus) utilizing bioflocs technology. International Biodeterioration and Biodegradation 102: 100-106.

Al-Khafaji, F.M., Romano, N., Nurul Amin, S.M., Fadel, A.H.I., Ebrahimi, M., Karami, A. & Arshad, A. 2017. Effects of feeding frequencies on the growth, plasma biochemistry, and liver glycogen of jade perch Scortum barcoo in a recirculating system. North American Journal of Aquaculture 79(3): 216-223.

Association of Official Analytic Chemists (AOAC). 2012. Official Methods of Analysis. Washington D.C.: United States.

Barragan-Fonseca, K.B., Dicke, M. & van Loon, J.J.A. 2017. Nutritional value of the black soldier fly (Hermetia illucens L.) and its suitability as animal feed - A review. Journal of Insects as Food and Feed 3(2): 105-120.

Barroso, F.G., de Haro, C., Sánchez-Muros, M.J., Venegas, E., Martínez-Sánchez, A. & Pérez-Bañón, C. 2014. The potential of various insect species for use as food for fish. Aquaculture 422: 193-201.

Belghit, I., Liland, N.S., Gjesdal, P., Biancarosa, I., Menchetti, E., Li, Y., Waagbø, R., Krogdahl, Å. & Lock, E.J. 2019. Black soldier fly larvae meal can replace fish meal in diets of sea-water phase Atlantic salmon (Salmo salar). Aquaculture 503: 609-619.

Besson, M., Komen, H., Rose, G. & Vandeputte, M. 2020. The genetic correlation between feed conversion ratio and growth rate affects the design of a breeding program for more sustainable fish production. Genetics Selection Evolution 52: 5.

Borgogno, M., Dinnella, C., Iaconisi, V., Fusi, R., Scarpaleggia, C., Schiavone, A., Monteleone, E., Gasco, L. & Parisi, G. 2017. Inclusion of Hermetia illucens larvae meal on rainbow trout (Oncorhynchus mykiss) feed: Effect on sensory profile according to static and dynamic evaluations. Journal of the Science of Food and Agriculture 97(10): 3402-3411.

Boyd, C.E. & Mcnevin, A.A. 2023. Resource use and pollution potential in feed-based aquaculture. Reviews in Fisheries Science & Aquaculture DOI: 10.1080/23308249.2023.2258226

Boyd, C.E., McNevin, A.A. & Davis, R.P.  2022. The contribution of fisheries and aquaculture to the global protein supply. Food Security 14(3): 805-827.

Deng, Y., Borewicz, K., van Loo, J., Zabala, M., Fotini, O. & Detmer, K. 2022. In-situ biofloc affects the core prokaryotes community composition in gut and enhances growth of Nile tilapia (Oreochromis niloticus). Microbial Ecology 84: 879-892.

Dong, S., Li, Y., Jiang, F., Hu, Z. & Zheng, Y. 2021. Performance of Platymonas and microbial community analysis under different C/N ratio in biofloc technology aquaculture system. Journal of Water Process Engineering 43: 102257.

Du, Z.Y. & Turchini, G.M. 2022. Are we actually measuring growth? - An appeal to use a more comprehensive growth index system for advancing aquaculture research. Reviews in Aquaculture 14(2): 525-527.

Fu, G. & Yuna, Y. 2022. Phenotyping and phenomics in aquaculture breeding. Aquaculture and Fisheries 7(2): 140-146.

Guerreiro, I., Castro, C., Antunes, B., Coutinho, F., Rangel, F., Couto, A., Serra, C.R., Peres, H., Pousão-Ferreira, P., Matos, E., Gasco, L., Gai, F., Corraze, G., Oliva-Teles, A. & Enes, P. 2020. Catching black soldier fly for meagre: Growth, whole-body fatty acid profile and metabolic responses. Aquaculture 516: 734613.

Kalva, J.J., Sims, C.A., Puentes, L.A., Snyder, D.J. & Bartoshuk, L.M. 2014. Comparison of the hedonic general labeled magnitude scale with the hedonic 9-point scale. Journal of Food Science 79(2): S238-S245.

Li, X., Zheng, S. & Wu, G. 2021. Nutrition and functions of amino acids in fish. In Amino Acids in Nutrition and Health: Amino Acids in the Nutrition of Companion, Zoo and Farm Animals, edited by Wu, G. Cham: Springer International Publishing. pp. 133-168.

Li, C., Zhang, X., Chen, Y., Zhang, S., Dai, L., Zhu, W. & Chen, Y. 2023. Optimized utilization of organic carbon in aquaculture biofloc systems: A review. Fishes 8(9): 465.

Lock, E.R., Arsiwalla, T. & Waagbø, R. 2016. Insect larvae meal as an alternative source of nutrients in the diet of Atlantic salmon (Salmo salar) postsmolt. Aquaculture Nutrition 22(6): 1202-1213.

Luo, G., Zhang, N. & Tan, H. 2012. Effect of low salinity on jade perch Scortum barcoo performance in a recirculating aquaculture system. North American Journal of Aquaculture 74(3): 395-399.

Mancini, S., Medina, I., Iaconisi, V., Gai, F., Basto, A. & Parisi, G. 2018. Impact of black soldier fly larvae meal on the chemical and nutritional characteristics of rainbow trout fillets. Animal 12(8): 1672-1681.

Menaga, M., Felix, S., Charulatha, M., Gopalakannan, A. & Panigrahi, A. 2019. Effect of in-situ and ex-situ biofloc on immune response of genetically improved farmed tilapia. Fish and Shellfish Immunology 92: 698-705.

Mikołajczak, Z., Rawski, M., Mazurkiewicz, J., Kierończyk, B., Kołodziejski, P., Pruszyńska-Oszmałek, E. & Józefiak, D. 2022. The first insight into black soldier fly meal in brown trout nutrition as an environmentally sustainable fish meal replacement. Animal 16(5): 100516.

Minabi, K., Sourinejad, I., Alizadeh, M., Ghatrami, E.R. & Khanjani, M.H. 2020. Effects of different carbon to nitrogen ratios in the biofloc system on water quality, growth, and body composition of common carp (Cyprinus carpio L.) fingerlings. Aquaculture International 28(5): 1883-1898.

Mo, W.Y., Man, Y.B., Zhang, F. & Wong, M.H. 2019. Fermented food waste for culturing jade perch and Nile tilapia: Growth performance and health risk assessment based on metal/loids. Journal of Environmental Management 236: 236-244.

Moutinho, S., Pedrosa, R., Magalhães, R., Oliva-Teles, A., Parisi, G. & Peres, H. 2021. Black soldier fly (Hermetia illucens) pre-pupae larvae meal in diets for European seabass (Dicentrarchus labrax) juveniles: Effects on liver oxidative status and fillet quality traits during shelf-life. Aquaculture 533: 736080.

Mugwanya, M., Dawood, M.A.O., Kimera, F. & Sewilam, H. 2021. Biofloc systems for sustainable production of economically important aquatic species: A review. Sustainability 13(13): 7255.

Muin, H., Taufek, N.M., Alias, Z. & Nor, A.M. 2023. Supplementation of red seaweed (Gracilaria changii) in black soldier fly (Hermetia illucens) larvae-based diet for red hybrid tilapia: Effects on growth performance, fillet quality, sensory analysis, haematological indices, and antioxidant enzyme activiti. Journal of Applied Phycology 35(5): 2495-2509.

Muin, H., Alias, Z., Md. Nor, A. & Mohd Taufek, N. 2022. Bioconversion of desiccated coconut and soybean curd residues for enhanced black soldier fly larvae biomass as a circular bioeconomy approach. Waste and Biomass Valorization 14: 249-260.

Muin, H., Taufek, N.M., Kamarudin, M.S. & Razak, S.A. 2017. Growth performance, feed utilization and body composition of Nile tilapia, Oreochromis niloticus (Linnaeus, 1758) fed with different levels of black soldier fly, Hermetia illucens (Linnaeus, 1758) maggot meal diet. Iranian Journal of Fisheries Sciences 16(2): 567-577.

Navarro, A., De Cássia, R., Aurélio, M., Ferreira, M., Paula, V., Minim, R., De Melo, T. & Perez, R. 2013. Performance of hedonic scales in sensory acceptability of strawberry yogurt. Food Quality and Preference 30(1): 9-21.

Ordoñez, B.M., Santana, T.M., Carneiro, D.P., dos Santos, D.K.M., Parra, G.A.P., Moreno, L.C.C., Teixeira Filho, N.P., Aguilar, F.A.A., Yamamoto, F.Y. & Gonçalves, L.U. 2022. Whole black soldier fly larvae (Hermetia illucens) as dietary replacement of extruded feed for tambaqui (Colossoma macropomum) juveniles. Aquaculture Journal 2(4): 246-256.

Panigrahi, A., Sundaram, M., Chakrapani, S., Rajasekar, S., Syama Dayal, J. & Chavali, G.  2019. Effect of carbon and nitrogen ratio (C:N) manipulation on the production performance and immunity of Pacific white shrimp Litopenaeus vannamei (Boone, 1931) in a biofloc-based rearing system. Aquaculture Research 50(1): 29-41.

Peryam, D.R. & Pilgrim, F.J. 1957. Hedonic scale method of measuring food preferences. Food Technology 11: 9-14.

Song, L.P., Zhu, Y.A. & Wang, A.Y. 2009. Effects of dietary lipids on growth and feed utilization of jade perch, Scortum barcoo. Journal of the World Aquaculture Society 40(2): 266-273.

Prakoso, V.A., Irawan, A., Iswantari, A., Maulana, F., Samsudin, R. & Jayanegara, A. 2022. Evaluation of dietary inclusion of black soldier fly (Hermetia illucens) larvae on fish production performance: A meta-analysis. Journal of Insects as Food and Feed 8(11): 1373-1384.

Rawski, M., Mazurkiewicz, J., Kierończyk, B. & Józefiak, D. 2020. Black soldier fly full-fat larvae meal as an alternative to fish meal and fish oil in Siberian sturgeon nutrition: The effects on physical properties of the feed, animal growth performance, and feed acceptance and utilization. Animals 10(11): 1-19.

Renna, M., Schiavone, A., Gai, F., Dabbou, S., Lussiana, C., Malfatto, V., Prearo, M., Capucchio, M.T., Biasato, I., Biasibetti, E., De Marco, M., Brugiapaglia, A., Zoccarato, I. & Gasco, L. 2017. Evaluation of the suitability of a partially defatted black soldier fly (Hermetia illucens L.) larvae meal as ingredient for rainbow trout (Oncorhynchus mykiss Walbaum) diets. Journal of Animal Science and Biotechnology 8(1): 1-13.

Rind, K.H., Habib, S.S., Ujan, J.A., Fazio, F., Naz, S., Batool, A.I., Ullah, M., Attaullah, S., Khayyam, K. & Khan, K. 2023. The effects of different carbon sources on water quality, growth performance, hematology, immune, and antioxidant status in cultured Nile tilapia with biofloc technology. Fishes 8(10): 512.

Ruiz-Capillas, C. & Moral, A. 2001. Changes in free amino acids during chilled storage of hake (Merluccius merluccius L) in controlled atmospheres and their use as a quality control index. European Food Research and Technology 212(3): 302-307.

Schulz, C., Huber, M., Ogunji, J. & Rennert, B. 2008. Effects of varying dietary protein to lipid ratios on growth performance and body composition of juvenile pike perch (Sander lucioperca). Aquaculture Nutrition 14(2): 166-173.

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.

Siva Raman, S., Stringer, L.C., Bruce, N.C. & Chong, C.S. 2022. Opportunities, challenges and solutions for black soldier fly larvae-based animal feed production. Journal of Cleaner Production 373: 133802.

Stejskal, V., Tran, H.Q., Prokesová, M., Zare, M., Gebauer, T., Policar, T., Caimi, C., Gai, F. & Gasco, L. 2023. Defatted black soldier fly (Hermetia illucens) in pikeperch (Sander lucioperca) diets: Effects on growth performance, nutrient digestibility, fillet quality, economic and environmental sustainability. Animal Nutrition 12: 7-19.

Taufek, N.M., Lim, J.Z.Y. & Bakar, N.H.A. 2021. Comparative evaluation of Hermetia illucens larvae reared on different substrates for red tilapia diet: Effect on growth and body composition. Journal of Insects as Food and Feed 7(1): 79-88.

Tran, H.Q., von Siebenthal, E.W., Luce, J.B., Nguyen, T.T., Stejskal, V., Weinlaender, F. & Janssens, T. 2024. A novel protein source from lesser mealworm (Alphitobius diaperinus) larvae meal for European perch (Perca fluviatilis): Investigation on pellet characteristics, production performance, serum biochemistry, digestibility, histology, sensory and trait of fillet, and environmental indices. Aquaculture 581: 740460.

Tschirner, M. & Simon, A. 2015. Influence of different growing substrates and processing on the nutrient composition of black soldier fly larvae destined for animal feed. Journal of Insects as Food and Feed 1(4): 249-259.

Van Hoestenberghe, S., Fransman, C.A., Luyten, T., Vermeulen, D., Roelants, I., Buysens, S. & Goddeeris, B.M. 2016. Schizochytrium as a replacement for fish oil in a fishmeal free diet for jade perch, Scortum barcoo (McCulloch & Waite). Aquaculture Research 47(6): 1747-1760.

Van Hoestenberghe, S., Roelants, I., Vermeulen, D. & Goddeeris, B.M. 2013. Total replacement of fish oil with vegetable oils in the diet of juvenile jade perch. Journal of Agriculture Science and Technology 3: 385-398.

van Huis, A., Oonincx, D.G.A.B., Rojo, S. & Tomberlin, J.K. 2020. Insects as feed: House fly or black soldier fly? Journal of Insects as Food and Feed 6(3): 221-229.

Vongvichith, B., Morioka, S., Sugita, T., Phousavanh, N., Phetsanghanh, N., Chanthasone, P., Pommachan, P. & Nakamura, S. 2020. Evaluation of the efficacy of aquaculture feeds for the climbing perch Anabas testudineus: Replacement of fishmeal by black soldier fly Hermetia illucens prepupae. Fisheries Science 86(1): 145-151.

Xie, X., Ye, G., Bao, Y., Ying, Z., Xie, M., Zhu, C. & Wang, R. 2021. Effects of starvation stress on jade perch Scortum barcoo based on proteomics analysis. Aquaculture Research 52(6): 2840-2851.

Xu, X., Ji, H., Belghit, I. & Sun, J. 2020. Black soldier fly larvae as a better lipid source than yellow mealworm or silkworm oils for juvenile mirror carp (Cyprinus carpio var. specularis). Aquaculture 527: 735453.

Yang, P., Yao, W., Wang, Y., Li, M., Li, X. & Leng, X. 2022. Dietary effects of fish meal substitution with Clostridium autoethanogenum on flesh quality and metabolomics of largemouth bass (Micropterus salmoides). Aquaculture Reports 23: 101012.

Yu, Y.B., Choi, J.H., Lee, J.H., Jo, A.H., Lee, K.M. & Kim, J.H. 2023. Biofloc technology in fish aquaculture: A review. Antioxidants 12(2): 398.

Zarantoniello, M., Zimbelli, A., Randazzo, B., Compagni, M.D., Truzzi, C., Antonucci, M., Riolo, P., Loreto, N., Osimani, A., Milanović, V., Giorgini, E., Cardinaletti, G., Tulli, F., Cipriani, R., Gioacchini, G. & Olivotto, I. 2020. Black soldier fly (Hermetia illucens) reared on roasted coffee by-product and Schizochytrium sp. as a sustainable terrestrial ingredient for aquafeeds production. Aquaculture 518: 734659.

*Pengarang untuk surat-menyurat; email: hidayah.taufek@um.edu.my