Animal Bioscience

Asian Australasian Association of Animal Production Societies (아세아태평양축산학회)
권호 표지
DOI QR코드

DOI QR Code

Insect meal as a feed ingredient for poultry

  • Elahi, Usman (Key Laboratory of Feed Biotechnology, Ministry of Agriculture and Rural Affairs, National Engineering Research Center of Biological Feed, Feed Research Institute, Chinese Academy of Agricultural Sciences) ;
  • Xu, Chang-chun (Key Laboratory of Feed Biotechnology, Ministry of Agriculture and Rural Affairs, National Engineering Research Center of Biological Feed, Feed Research Institute, Chinese Academy of Agricultural Sciences) ;
  • Wang, Jing (Key Laboratory of Feed Biotechnology, Ministry of Agriculture and Rural Affairs, National Engineering Research Center of Biological Feed, Feed Research Institute, Chinese Academy of Agricultural Sciences) ;
  • Lin, Jing (Key Laboratory of Feed Biotechnology, Ministry of Agriculture and Rural Affairs, National Engineering Research Center of Biological Feed, Feed Research Institute, Chinese Academy of Agricultural Sciences) ;
  • Wu, Shu-geng (Key Laboratory of Feed Biotechnology, Ministry of Agriculture and Rural Affairs, National Engineering Research Center of Biological Feed, Feed Research Institute, Chinese Academy of Agricultural Sciences) ;
  • Zhang, Hai-jun (Key Laboratory of Feed Biotechnology, Ministry of Agriculture and Rural Affairs, National Engineering Research Center of Biological Feed, Feed Research Institute, Chinese Academy of Agricultural Sciences) ;
  • Qi, Guang-hai (Key Laboratory of Feed Biotechnology, Ministry of Agriculture and Rural Affairs, National Engineering Research Center of Biological Feed, Feed Research Institute, Chinese Academy of Agricultural Sciences)
  • Received : 2021.09.23
  • Accepted : 2021.11.16
  • Published : 2022.02.01
Download PDF
⟨ Previous Next ⟩

Abstract

Shortage of protein feed resources is the major challenge to the world farm animal industry. Insects are known as an alternative protein source for poultry. A wide range of insects are available for use in poultry diets. Insect larvae thrive in manure, and organic waste, and produce antimicrobial peptides to protect themselves from microbial infections, and additionally these peptides might also be functional in poultry feed. The feed containing antimicrobial peptides can improve the growth performance, nutrient digestibility, intestinal health, and immune function in poultry. Insect meal contains a higher amount of essential amino acids compared to conventional feedstuffs. Black soldier fly, mealworm, housefly, cricket/Grasshopper/Locust (Orthoptera), silkworm, and earthworm are the commonly used insect meals in broiler and laying hen diets. This paper summarizes the nutrient profiles of the insect meals and reviews their efficacy when included in poultry diets. Due to the differences in insect meal products, and breeds of poultry, inconsistent results were noticed among studies. The main challenge for proper utilization, and the promising prospect of insect meal in poultry diet are also addressed in the paper. To fully exploit insect meal as an alternative protein resource, and exert their functional effects, modes of action need to be understood. With the emergence of more accurate and reliable studies, insect meals will undoubtedly play more important role in poultry feed industry.

Keywords

Acknowledgement

The authors are grateful for the support by Beijing Innovation Consortium of Agriculture Research System Poultry-related Science and Technology Team (CARS-PSTP), Shandong Key Science and Technology Innovation Program (2019JZZY010704) and Agricultural Science and Technology Innovation Program of the Chinese Academy of Agricultural Sciences (CAAS-ASTPI-2017-FRI-03).

References

  1. Chavez M, Uchanski M. Insect left-over substrate as plant fertiliser. J Insects Food Feed 2021;7:683-694. https://doi.org/10.3920/JIFF2020.0063
  2. Slade EM, Riutta T, Roslin T, Tuomisto HL. The role of dung beetles in reducing greenhouse gas emissions from cattle farming. Sci Rep-Uk 2021;6:18140. https://doi.org/10.1038/srep18140
  3. Veldkamp T, Bosch G. Insects - a protein rich feed ingredient in pig and poultry diets. Anim Front 2015;5:45-50.
  4. Al-qazzaz MF, Ismail DB. Insect meal as a source of protein in animal diet. Anim Nutr Feed Technnol 2016;16:527-547. https://doi.org/10.5958/0974-181X.2016.00038.X
  5. Khan SH. Recent advances in role of insects as alternative protein source in poultry nutrition. J Appl Anim Res 2018; 46:1144-57. https://doi.org/10.1080/09712119.2018.1474743
  6. Elahi U, Wang J, Ma Y, et al. Evaluation of yellow mealworm meal as a protein feedstuff in the diet of broiler chicks. Animals 2020;10:224. https://doi.org/10.3390/ani10020224
  7. Kroncke N, Grebenteuch S, Keil C, et al. Effect of different drying methods on nutrient quality of the yellow mealworm (Tenebrio molitor L.). Insects 2019;10:84. https://doi.org/10.3390/insects10040084
  8. Gasco L, Finke M, van Huis A. Can diets containing insects promote animal health? J Insects Food Feed 2018;4:1-4. https://doi.org/10.3920/JIFF2018.x001
  9. Lee CG, Da Silva CA, Lee JY, Hartl D, Elias JA. Chitin regulation of immune responses: an old molecule with new roles. Curr Opin Immunol 2008;20:684-689. https://doi.org/10.1016/j.coi.2008.10.002
  10. Chu X, Li M, Wang G, et al. Evaluation of the low inclusion of full-fatted hermetia illucens larvae meal for layer chickens: growth performance, nutrient digestibility, and gut health. Front Vet Sci 2020;7:585843. https://doi.org/10.3389/fvets.2020.585843
  11. Schiavone A, De Marco M, Martinez S, et al. Nutritional value of a partially defatted and a highly defatted black soldier fly larvae (Hermetia illucens L.) meal for broiler chickens: apparent nutrient digestibility, apparent metabolizable energy and apparent ileal amino acid digestibility. J Anim Sci Biotechnol 2017;8:51. https://doi.org/10.1186/s40104-017-0181-5
  12. Bovera F, Piccolo G, Gasco L, et al. Yellow mealworm larvae (Tenebrio molitor, L.) as a possible alternative to soybean meal in broiler diets. Br Poult Sci 2015;56:569-575. https://doi.org/10.1080/00071668.2015.1080815
  13. Khempaka S, Chitsatchapong C, Molee W. Effect of chitin and protein constituents in shrimp head meal on growth performance, nutrient digestibility, intestinal microbial populations, volatile fatty acids, and ammonia production in broilers. J Appl Poult Res 2011;20:1-11. https://doi.org/10.3382/japr.2010-00162
  14. Menconi A, Pumford NR, Morgan MJ, et al. Effect of chitosan on Salmonella Typhimurium in broiler chickens. Foodborne Path Dis 2014;11:165. https://doi.org/10.1089/fpd.2013.1628
  15. Makkar HPS, Tran G, Heuze V, Ankers P. State-of-the-art on use of insects as animal feed. Anim Feed Sci Technol 2014;197:1-33. https://doi.org/10.1016/j.anifeedsci.2014.07.008
  16. Eilenberg J, Vlak JM, Nielsen-LeRoux C, Cappellozza S, Jensen AB. Diseases in insects produced for food and feed. J Insects Food Feed 2015;1:87-102. https://doi.org/10.3920/JIFF2014.0022
  17. Jozefiak A, Engberg RM. Insect proteins as a potential source of antimicrobial peptides in livestock production. A review. J Anim Feed Sci 2017;26:87-99. https://doi.org/10.22358/jafs/69998/2017
  18. Mancini S, Fratini F, Tuccinardi T, Degl'Innocenti C, Paci G. Tenebrio molitor reared on different substrates: is it gluten free? Food Control 2020;110:107014. https://doi.org/10.1016/j.foodcont.2019.107014
  19. Charlton AJ, Dickinson M, Wakefield ME, et al. Exploring the chemical safety of fly larvae as a source of protein for animal feed. J Insects Food Feed 2015;1:7-16. https://doi.org/10.3920/JIFF2014.0020
  20. Choi YC, Park KH, Nam SH, et al. The effect on growth performance of chicken meat in broiler chicks by dietary supplementation of black soldier fly larvae, Hermetia illucens (Diptera: Stratmyidae). J Sericult Entomol Sci 2013;51:30-35. https://doi.org/10.7852/jses.2013.51.1.30
  21. Wang S, Zeng X, Yang Q, Qiao S. Antimicrobial peptides as potential alternatives to antibiotics in food animal industry. Int J Mol Sci 2016;17:603. https://doi.org/10.3390/ijms17050603
  22. Van Huis A. Insects as food and feed, a new emerging agricultural sector: a review. J Insects Food Feed 2020;6:27-44. https://doi.org/10.3920/JIFF2019.0017
  23. Nekrasov RV, Zelenchenkova AA, Chabaev MG, Ushakova NA. Melanine protein-energy additive from Hermetia illucens larvae in nutrition of calves. Sel'skokhozyaistvennaya Biol 2018;53:374-384. https://doi.org/10.15389/agrobiology.2018.2.374eng
  24. Ushakova NA, Dontsov AE, Sakina NL, et al. Melanin and melanogenesis at different life stages in Hermetia illucens. Biol Bull 2018;45:47-50. https://doi.org/10.1134/S1062359018010120
  25. Lieberman S, Enig MG, Preuss HG. A review of monolaurin and lauric acid: Natural virucidal and bactericidal agents. Altern Complement Ther 2006;12:310-314. http://doi.org/10.1089/act.2006.12.310
  26. Sun T, Long RJ, Liu ZY. The effect of a diet containing grasshoppers and access to free-range on carcase and meat physicochemical and sensory characteristics in broilers. Br Poult Sci 2013;54:130-137. https://doi.org/10.1080/00071668.2012.756575
  27. Iqbal A, Qudoos A, Cetingul IS, Shah SRA, Bayram I. Insects as alternative feed materials for poultry nutrition. J Anim Sci Prod 2019;2:30-37.
  28. Kawasaki K, Hashimoto Y, Hori A, et al. Evaluation of black soldier fly (Hermetia illucens) larvae and Pre-Pupae raised on household organic waste, as potential ingredients for poultry feed. Animals 2019;9:98. https://doi.org/10.3390/ani9030098
  29. Nyakeri EM, Ogola HJ, Ayieko MA, Amimo FA. An open system for farming black soldier fly larvae as a source of proteins for smallscale poultry and fish production. J Insects Food Feed 2017;3:51-6. https://doi.org/10.3920/JIFF2016.0030
  30. Liu X, Liu X, Yao Y, et al. Effects of different levels of Hermetia illucens larvae meal on performance, egg quality, yolk fatty acid composition and oxidative status of laying hens. Ital J Anim Sci 2021;20:256-266. https://doi.org/10.1080/1828051X.2021.1878946
  31. De Marco M, Martinez S, Hernandez F, et al. Nutritional value of two insect larval meals (Tenebrio molitor and Hermetia illucens) for broiler chickens: Apparent nutrient digestibility, apparent ileal amino acid digestibility and apparent metabolizable energy. Anim Feed Sci Technol 2015;209:211-218. https://doi.org/10.1016/j.anifeedsci.2015.08.006
  32. Vilela J de S, Alvarenga TIRC, Andrew NR, et al. Technological quality, amino acid and fatty acid profile of broiler meat enhanced by dietary inclusion of black soldier fly larvae. Foods 2021;10:297. https://doi.org/10.3390/foods10020297
  33. Mohammed A, Laryea TE, Ganiyu A, Adongo T. Effects of black soldier fly (hermetia illucens) larvae meal on the growth performance of broiler chickens. Intl J Dev 2017;4:35-41.
  34. Onsongo VO, Osuga IM, Gachuiri CK, et al. Insects for income generation through animal feed: effect of dietary replacement of soybean and fish meal with black soldier fly meal on broiler growth and economic performance. J Econ Entomol 2018;111:1966-1973. https://doi.org/10.1093/jee/toy118
  35. Biasato I, Ferrocino I, Dabbou S, et al. Black soldier fly and gut health in broiler chickens: insights into the relationship between cecal microbiota and intestinal mucin composition. J Anim Sci Biotechnol 2020;11:1-12. https://doi.org/10.1186/s40104-019-0409-7
  36. Mwaniki Z, Neijat M, Kiarie E. Egg production and quality responses of adding up to 7.5% defatted black soldier fly larvae meal in a corn-soybean meal diet fed to Shaver White Leghorns from wk 19 to 27 of age. Poult Sci 2018;97:2829-2835. https://doi.org/10.3382/ps/pey118
  37. Neumann C, Velten S, Liebert F. Improving the dietary protein quality by amino acid fortification with a high inclusion level of micro algae (Spirulina platensis) or insect meal (Hermetia illucens) in meat type chicken diets. Open J Anim Sci 2018;8: 12-26. https://doi.org/10.4236/ojas.2018.81002
  38. Neumann C, Velten S, Liebert F. The graded inclusion of algae (Spirulina platensis) or insect (Hermetia illucens) meal as a soybean meal substitute in meat type chicken diets impacts on growth, nutrient deposition and dietary protein quality depending on the extent of amino acid Supplementation. Open J Anim Sci 2018;8:163-183. https://doi.org/10.4236/ojas.2018.82012
  39. Brede A, Wecke C, Liebert F. Does the optimal dietary methionine to cysteine ratio in diets for growing chickens respond to high inclusion rates of insect meal from Hermetia illucens? Animals 2018;8:187. https://doi.org/10.3390/ani8110187
  40. Rothstein S. Potential of Hermetia illucens larvae meal as protein source in broiler diets [Internet]. Lohmann Information [cited 2021 Sept 18]. Available from: https://lohmann-breeders.com/lohmanninfo/potential-of-hermetia-illucens-larvae-meal-as-protein-source-in-broiler-diets/
  41. Moula N, Scippo ML, Douny C, et al. Performances of local poultry breed fed black soldier fly larvae reared on horse manure. Anim Nutr 2018;4:73-78. https://doi.org/10.1016/j.aninu.2017.10.002
  42. Oonincx DGABAB. Insects as food and feed: Nutrient composition and environmental impact. Wageningen, The Netherlands: Wageningen University; 2015.
  43. Newton GL, Sheppard DC, Watson DW, et al. The black soldier fly, Hermetia illucens, as a manure management / resource recovery tool. In: Symposium on the state of the science of Animal Manure and Waste Management; 2005. 57 p.
  44. Van Huis A. Edible insects. Future prospects for food and feed security [Internet]. Vol. 171, Rome, Italy: Food and Agriculture Organization of the United Nations; 2013. 201 p. Available from: http://www.fao.org/3/i3253e/i3253e00.htm
  45. Veldkamp T, van Duinkerken G, van Huis A, et al. Insects as a sustainable feed ingredient in pig and poultry diets - a feasibility study. Wageningen, The Netherlands: Wageningen UR Livestock Research; 2012.
  46. Dahiru S, Azhar B, Anjas AB. Performance of Spring chicken fed different inclusion levels of black soldier fly larvae meal. Entomol Ornithol Herpetol 2016;5:185. https://doi.org/10.4172/2161-0983.1000185
  47. Schiavone A, Dabbou S, Petracci M, et al. Black soldier fly defatted meal as a dietary protein source for broiler chickens: effects on carcass traits, breast meat quality and safety. Animal 2019;13:2397-2405. https://doi.org/10.1017/S1751731119000685
  48. Dabbou S, Gai F, Biasato I, et al. Black soldier fly defatted meal as a dietary protein source for broiler chickens: effects on growth performance, blood traits, gut morphology and histological features. J Anim Sci Biotechnol 2018;9:49. https://doi.org/10.1186/s40104-018-0266-9
  49. Kareem KY, Abdulla NR, Foo HL, et al. Effect of feeding larvae meal in the diets on growth performance, nutrient digestibility and meat quality in broiler chicken. Indian J Anim Sci 2018;88:1180-1185. https://doi.org/10.56093/ijans.v88i10.84155
  50. Lee J, Kim YM, Park YK, Yang YC, Jung BG, Lee BJ. Black soldier fly (Hermetia illucens) larvae enhances immune activities and increases survivability of broiler chicks against experimental infection of Salmonella Gallinarum. J Vet Med Sci 2018;80:736-740. https://doi.org/10.1292/jvms.17-0236
  51. Manangkot HJ, Rondonuwu SJ, Pinontoan OR, Najoan M, Rumokoy JM. Black soldier fly larvae manure degradation as fish meal replacer in native chicken ration. Lucrari Stiintifice - Seria Zootehnie 2014;62:139-142.
  52. Mohammed A. Evaluation of black soldier fly (Hermetia illucens) larvae meal as an alternative protein source in broiler chicken diets: effect on carcass and eating quality of broiler chicken. Research & Reviews: J Food Sci Technol 2017;6:18-21.
  53. Pieterse E, Erasmus S, Hoffman LC. Black soldier fly (Hermetia illucens) pre-pupae meal as a dietary protein source for broiler production ensures a tasty chicken with standard meat quality for every pot. J Sci Food Agric 2019;99:893-903. https://doi.org/10.1002/jsfa.9261
  54. Schiavone A, Dabbou S, De Marco M, et al. Black soldier fly larva fat inclusion in finisher broiler chicken diet as an alternative fat source. Animal 2018;12:2032-2039. https://doi.org/10.1017/S1751731117003743
  55. Schiavone A, Cullere M, De Marco M, et al. Partial or total replacement of soybean oil by black soldier fly larvae (Hermetia illucens L.) fat in broiler diets: effect on growth performances, feed-choice, blood traits, carcass characteristics and meat quality. Ital J Anim Sci 2017;16:93-100. https://doi.org/10.1080/1828051X.2016.1249968
  56. Cullere M, Schiavone A, Dabbou S, Gasco L, Dalle Zotte A. Meat quality and sensory traits of finisher broiler chickens fed with black soldier fly (Hermetia Illucens L.) larvae fat as alternative fat source. Animals 2019;9:140. https://doi.org/10.3390/ani9040140
  57. Leiber F, Gelencser T, Stamer A, et al. Insect and legume-based protein sources to replace soybean cake in an organic broiler diet: Effects on growth performance and physical meat quality. Renew Agric Food Syst 2017;32:21-7. https://doi.org/10.1017/S1742170515000496
  58. Heuel M, Sandrock C, Leiber F, et al. Black soldier fly larvae meal and fat can completely replace soybean cake and oil in diets for laying hens. Poult Sci 2021;100:101034. https://doi.org/10.1016/j.psj.2021.101034
  59. Marono S, Loponte R, Lombardi P, et al. Productive performance and blood profiles of laying hens fed Hermetia illucens larvae meal as total replacement of soybean meal from 24 to 45 weeks of age. Poult Sci 2017;96:1783-90. https://doi.org/10.3382/ps/pew461
  60. Maurer V, Holinger M, Amsler Z, et al. Replacement of soybean cake by Hermetia illucens meal in diets for layers. J Insects Food Feed 2016;2:83-90. https://doi.org/10.3920/JIFF2015.0071
  61. Zadeh ZS, Kheiri F, Faghani M. Use of yellow mealworm (Tenebrio molitor) as a protein source on growth performance, carcass traits, meat quality and intestinal morphology of Japanese quails (Coturnix japonica). Vet Anim Sci 2019;8: 100066. https://doi.org/10.1016/j.vas.2019.100066
  62. Sedgh-Gooya S, Torki M, Darbemamieh M, Khamisabadi H, Karimi Torshizi MA, Abdolmohamadi A. Yellow mealworm, Tenebrio molitor (Col: Tenebrionidae), larvae powder as dietary protein sources for broiler chickens: Effects on growth performance, carcass traits, selected intestinal microbiota and blood parameters. J Anim Physiol Anim Nutr 2021; 105:119-28. https://doi.org/10.1111/jpn.13434
  63. Benzertiha A, Kieronczyk B, Kolodziejski P, et al. Tenebrio molitor and Zophobas morio full-fat meals as functional feed additives affect broiler chickens' growth performance and immune system traits. Poult Sci 2020;99:196-206. https://doi.org/10.3382/ps/pez450
  64. Khan S, Khan RU, Alam W, Sultan A. Evaluating the nutritive profile of three insect meals and their effects to replace soya bean in broiler diet. J Anim Physiol Anim Nutr 2018;102:e662-8. https://doi.org/10.1111/jpn.12809
  65. Islam MM, Yang CJ. Efficacy of mealworm and super mealworm larvae probiotics as an alternative to antibiotics challenged orally with Salmonella and E. coli infection in broiler chicks. Poult Sci 2017;96:27-34. https://doi.org/10.3382/ps/pew220
  66. Hussain I, Khan S, Sultan A, et al. Meal worm (Tenebrio molitor) as potential alternative source of protein supplementation in broiler. Int J Biosci 2017;10:255-62. https://doi.org/10.12692/ijb/10.4.255-262
  67. Benzertiha A, Kieronczyk B, Rawski M, et al. Tenebrio molitor and Zophobas morio full-fat meals in broiler chicken diets: effects on nutrients digestibility, digestive enzyme activities, and cecal microbiome. Animals 2019;9:1128. https://doi.org/10.3390/ani9121128
  68. Biasato I, Ferrocino I, Grego E, et al. Gut microbiota and mucin composition in female broiler chickens fed diets including yellow mealworm (Tenebrio molitor, L.). Animals 2019; 9:213. https://doi.org/10.3390/ani9050213
  69. Dabbou S, Gasco L, Lussiana C, et al. Yellow mealworm (Tenebrio molitor L.) larvae inclusion in diets for free-range chickens: effects on meat quality and fatty acid profile. Renew Agric Food Syst 2020;35:571-8. https://doi.org/10.1017/S1742170519000206
  70. Loponte R, Bovera F, Piccolo G, et al. Fatty acid profile of lipids and caeca volatile fatty acid production of broilers fed a full fat meal from Tenebrio molitor larvae. Ital J Anim Sci 2019;18:168-73. https://doi.org/10.1080/1828051X.2018.1502053
  71. Biasato I, Gasco L, De Marco M, et al. Yellow mealworm larvae (Tenebrio molitor) inclusion in diets for male broiler chickens: effects on growth performance, gut morphology, and histological findings. Poult Sci 2018;97:540-8. https://doi.org/10.3382/ps/pex308
  72. Biasato I, Gasco L, De Marco M, et al. Effects of yellow mealworm larvae (Tenebrio molitor) inclusion in diets for female broiler chickens: implications for animal health and gut histology. Anim Feed Sci Technol 2017;234:253-63. https://doi.org/10.1016/j.anifeedsci.2017.09.014
  73. Biasato I, De Marco M, Rotolo L, et al. Effects of dietary Tenebrio molitor meal inclusion in free-range chickens. J Anim Physiol Anim Nutr 2016;100:1104-12. https://doi.org/10.1111/jpn.12487
  74. Bovera F, Loponte R, Marono S, et al. Use of Tenebrio molitor larvae meal as protein source in broiler diet: Effect on growth performance, nutrient digestibility, and carcass and meat traits. J Anim Sci 2016;94:639-47. https://doi.org/10.2527/jas.2015-9201
  75. Kim SG, Kim JE, Oh HK, et al. Feed supplementation of yellow mealworms (Tenebrio molitor L.) improves blood characteristics and meat quality in broiler. J Agric Sci Technol 2014; 49:9-18. https://doi.org/10.29335/tals.2014.49.9
  76. Ballitoc DA, Sun S. Ground yellow mealworms (Tenebrio molitor L.) feed supplementation improves growth performance and carcass yield characteristics in broilers. Open Sci Reposit Agric 2013;e23050425. https://doi.org/10.7392/openaccess.23050425
  77. Hall HN, O'Neill HVM, Scholey D, et al. Amino acid digestibility of larval meal (Musca domestica) for broiler chickens. Poult Sci 2018;97:1290-7. https://doi.org/10.3382/ps/pex433
  78. Radulovic S, Pavlovic M, Sefer D, et al. Effects of housefly larvae (Musca domestica) dehydrated meal on production performances and sensory properties of broiler meat. Thai J Vet Med 2018;48:63-70.
  79. Awoniyi TAM, Aletor VA, Aina JM. Performance of broiler - Chickens fed on maggot meal in place of fishmeal. Int J Poult Sci 2003;2:271-4. https://doi.org/10.3923/ijps.2003.271.274
  80. Khan S, Khan RU, Sultan A, Khan M, Hayat SU, Shahid MS. Evaluating the suitability of maggot meal as a partial substitute of soya bean on the productive traits, digestibility indices and organoleptic properties of broiler meat. J Anim Physiol Anim Nutr 2016;100:649-56. https://doi.org/10.1111/jpn.12419
  81. Dordevic M, Radenkovic-Damnjanovic B, Vucinic M, et al. Effects of substitution of fish meal with fresh and dehydrated larvae of the house fly (Musca domestica L) on productive performance and health of broilers. Acta Vet 2008;58:357-68. https://doi.org/10.2298/AVB0804357D
  82. Hwangbo J, Hong EC, Jang A, et al. Utilization of house flymaggots, a feed supplement in the production of broiler chickens. J Environ Biol 2009;30:609-14.
  83. Teguia A, Mpoame M, Okourou Mba JA. The production performance of broiler birds as affected by the replacement of fish meal by maggot meal in the starter and finisher diets. Tropicultura 2002;20:187-92.
  84. Okah U, Onwujiariri EB. Performance of finisher broiler chickens fed maggot meal as a replacement for fish meal. J Agric Technol 2012;8:471-7.
  85. Mbiba HF, Etchu KA, Ndamukong K. Performance of broiler chickens fed maggot meal as a protein substitute for fish meal. J Ethol Anim Sci 2019;2:1-11.
  86. Elahi U, Ma Y, Wu S, Wang J, Zhang H, Qi G. Growth performance, carcass characteristics, meat quality and serum profile of broiler chicks fed on housefly maggot meal as a replacement of soybean meal. J Anim Physiol Anim Nutr 2020;104:1075-84. https://doi.org/10.1111/jpn.13265
  87. Dillak SYFG, Suryatni NPF, Handayani HT, et al. The effect of fed maggot meal as a supplement in the commercial diets on the performance of finisher broiler chickens. IOP Conf Series: Earth Environ Sci 2019;260:012056. https://doi.org/10.1088/1755-1315/260/1/012056
  88. Aniebo AO, Erondu ES, Owen OJ. Proximate composition of housefly larvae (Musca domestica) meal generated from mixture of cattle blood and wheat bran. Livest Res Rural Dev 2008;20:Article #205.
  89. Aniebo AO, Owen OJ. Effects of age and method of drying on the proximate composition of housefly larvae (Musca domestica Linnaeus) meal (HFLM). Pak J Nutr 2010;9:485-7. https://doi.org/10.3923/pjn.2010.485.487
  90. Khan M, Chand N, Khan S, Khan RU, Sultan A. Utilizing the house fly (Musca Domestica) larva as an alternative to soybean meal in broiler ration during the starter phase. Braz J Poult Sci 2018;20:9-14. https://doi.org/10.1590/1806-9061-2017-0529
  91. Ren JL, Wu YB, Lin JR. Effect of house fly larvae meal on growth performance and slaughter performance of yellow dwarf chickens. China Poult 2011;33:8-11.
  92. Pretorius Q. The evaluation of larvae of Musca domestica (common house fly) as protein source for broiler production. Stellenbosch, South Africa: Stellenbosch University;2011.
  93. Pieterse E, Pretorius Q, Hoffman LC, Drew DW. The carcass quality, meat quality and sensory characteristics of broilers raised on diets containing either Musca domestica larvae meal, fish meal or soya bean meal as the main protein source. Anim Prod Sci 2013;54:622-8. https://doi.org/10.1071/AN13073
  94. Chang B, Han RC, Cao L, Liu XFL, Liu XFL. Effect of Musca domestica maggot and pupae as feed additives on the quality and flavor of Qingyuan chickens. Chinese Bull Entomol 2007;44:882-6. https://doi.org/10.3969/j.issn.0452-8255.2007.06.023
  95. Dankwa DF, Nelson SEO, Oddoye K, Duncan JL. Housefly larvae as a feed supplement for rural poultry. Ghana J Agric Sci 2002;35:185-7.
  96. Agunbiade JA, Adeyemi OA, Ashiru OM, et al. Replacement of fish meal with maggot meal in cassava-based layers' diets. J Poult Sci 2007;44:278-82. https://doi.org/10.2141/jpsa.44.278
  97. Ghosh S, Haldar P, Mandal D. Evaluation of nutrient quality of a short horned grasshopper, Oxya hyla hyla Serville (Orthoptera: Acrididae) in search of new protein source. J Entomol Zool Stud 2016;4:193-7.
  98. Wang D, Zhai SW, Zhang CX, Zhang Q, Chen H. Nutrition value of the Chinese grasshopper Acrida cinerea (Thunberg) for broilers. Anim Feed Sci Technol 2007;135:66-74. https://doi.org/10.1016/j.anifeedsci.2006.05.013
  99. Nginya ES, Ondiek JO, King'ori AM, Nduko JM. Evaluation of grasshoppers as a protein source for improved indigenous chicken growers. Livest Res Rurual Dev 2019;31:Article #2.
  100. Brah N, Issa S, Houndonougbo F. Effect of grasshopper meal on laying hens' performance and eggs quality characteristics. Indian J Anim Sci 2017;87:1005-10.
  101. Amobi MI, Saleh A, Okpoko VO, Abdullahi AM. Growth performance of broiler chickens based on grasshopper meal inclusions in feed formulation. Zoologist 2020;18:39-43. https://doi.org/10.4314/tzool.v18i1.7
  102. Sanusi M, Garba A, Saidu I, Ali YZ. Performance of broiler chickens fed graded levels of grasshopper meals. Int J Appl Res Technol 2013;2:235-40.
  103. Sun T, Long RJ, Liu ZY, Ding WR, Zhang Y. Aspects of lipid oxidation of meat from free-range broilers consuming a diet containing grasshoppers on alpine steppe of the tibetan plateau. Poult Sci 2012;91:224-31. https://doi.org/10.3382/ps.2011-01598
  104. Ibitoye EB, Lokman IH, Hezmee MNM, et al. Gut health and serum growth hormone levels of broiler chickens fed dietary chitin and chitosan from cricket and shrimp. Poult Sci 2019;98:745-52. https://doi.org/10.3382/ps/pey419
  105. Longvah T, Mangthya K, Ramulu P. Nutrient composition and protein quality evaluation of eri silkworm (Samia ricinii) prepupae and pupae. Food Chem 2011;128:400-3. https://doi.org/10.1016/j.foodchem.2011.03.041
  106. Chieco C, Morrone L, Bertazza G, et al. The Effect of strain and rearing medium on the chemical composition, fatty acid profile and carotenoid content in Silkworm (Bombyx mori) pupae. Animals 2019;9:103. https://doi.org/10.3390/ani9030103
  107. Acay RP. Silkworm pupa meal as feed supplement for growing-finishing broilers. Benguet, Philippines: Benguet State University; 2011.
  108. Jintasataporn O. Production performance of broiler chickens fed with silkworm pupa (Bombyx mori). J Agric Sci TechnolIran 2012;2:505-10.
  109. Ijaiya AT, Eko EO. Effect of replacing dietary fish meal with silkworm (anaphe infracta) caterpillar meal on performance, carcass characteristics and haematological parameters of finishing broiler chicken. Pak J Biol Sci2009;8:850-5.
  110. Ullah R, Khan S, Khan N, et al. Replacement of soybean meal with silkworm meal in the diets of white leghorn layers and effects on performance, apparent total tract digestibility, blood profile and egg quality. Int J Vet Health Sci Res 2017;5: 200-7.
  111. Miah MY, Singh Y, Cullere M, Tenti S, Dalle Zotte A. Effect of dietary supplementation with full-fat silkworm (Bombyx mori L.) chrysalis meal on growth performance and meat quality of Rhode Island Red × Fayoumi crossbred chickens. Ital J Anim Sci 2020;19:447-56. https://doi.org/10.1080/1828051X.2020.1752119
  112. Ullah R, Khan S, Hafeez A, et al. Silkworm (Bombyx mori) meal as alternate protein ingredient in broiler finisher ration. Pak J Zool 2017;49:1463-70. https://doi.org/10.17582/journal.pjz/2017.49.4.1463.1470
  113. Istiqomah L, Sakti AA, Suryani AE, Karimy MF, Anggraeni AS, Herdian H. Effect of feed supplement containing earth-worm meal (Lumbricus rubellus) on production performance of quail (Coturnix coturnix japonica). IOP Conf Ser Earth Environ Sci 2017;101:012032. https://doi.org/10.1088/1755-1315/101/1/012032
  114. Jankovic LJ, Petrujkic B, Aleksic N, et al. Carcass characteristics and meat quality of broilers fed on earthworm (Lumbricus rubellus) meal. J Hellenic Vet Med Soc 2020;71: 2031-40. https://doi.org/10.12681/jhvms.22953
  115. Istiqomah L, Sofyan A, Damayanti E, Julendra H. Amino acid profile of earthworm and earthworm meal (Lumbricus Rubellus) for animal feedstuff. J Indonesian Trop Anim Agric 2009;34:253-7.
  116. Chashmidari Y, Esmaielzadeh L, Karimi-Torshizi MA, Seidavi A, da Silva Araujo CS, Araujo LF. Feed supplementation with vermi-humus and earthworm (Eisenia foetida) powder on broiler productivity. Ital J Anim Sci 2021;20:1054-62. https://doi.org/10.1080/1828051X.2021.1932615
  117. Bahadori Z, Esmaielzadeh L, Karimi-Torshizi MA, et al. The effect of earthworm (Eisenia foetida) meal with vermihumus on growth performance, hematology, immunity, intestinal microbiota, carcass characteristics, and meat quality of broiler chickens. Livest Sci 2017;202:74-81. https://doi.org/10.1016/j.livsci.2017.05.010
  118. Zang YT, Bing S, Zhang YZ, Sheng XW, Shu DQ. Effects of dietary supplementation with earthworm powder on production performance, blood characteristics, and heavy metal residues of broiler Pullets. J Appl Poult Res 2018;27:609-15. https://doi.org/10.3382/japr/pfy024
  119. Nalunga A, Komakech AJ, Jjagwe J, Magala H, Lederer J. Growth characteristics and meat quality of broiler chickens fed earthworm meal from Eudrilus eugeniae as a protein source. Livest Sci 2021;245:104394. https://doi.org/10.1016/j.livsci.2021.104394
  120. Gholami H, Shargh MS, Zarabi M, Zerehdaran S. Effect of different levels of earthworm meal (Eisenia Fetida) on performance, carcass characteristics and blood parameters of broiler chickens. Anim Prod Res 2016;7:70-6.
  121. Loh TC, Fong LY, Foo HL, Thanh NT, Sheikh-Omar AR. Utilisation of earthworm meal in partial replacement of soybean and fish meals in diets of broilers. J Appl Anim Res 2009;36:29-32. https://doi.org/10.1080/09712119.2009.9707024
  122. Musa U, Yusur J, Haruna ES, Karsin PD, Ali UD. Termites as possible animal protein supplement for Japanese quail (Coturnix coturnix Japonica) chicks feed. Nigerian J Biotechnol 2004;15:48-51.
  123. Pousga S, Sankara F, Coulibaly K, et al. Effects of replacement of fish meal by termites (Macrotermes sp.) on the weight evolution and the carcass characteristics of local poultry in Burkina Faso. Afr J Food Agric Nutr Dev 2019;19:14354-71. https://doi.org/10.18697/ajfand.85.17430
  124. Purwadari T, Ketaren PP, Sinurat AP, Sutikno I. Identification and evaluation of fiberhydrolytic enzymes in the extract of Termites (Glyptotermes montanus) for poultry feed application. Indonesian J Agric Sci 2003;4:40-7.
  125. Babarinde SA, Oladunjoye IO, Ojebiyi OO, Oyedeji SA. Inclusion of honey bee slum gum in broiler chicken feed. Int J Agric Biol 2011;13:781-5.
  126. Prakatur I, Miskulin I, Sencic D, et al. The influence of propolis and bee pollen on chicken meat quality. Vet Arhiv 2020;90:617-25. https://doi.org/10.24099/vet.arhiv.0888
  127. Prakatur I, Miskulin M, Pavic M, et al. Intestinal morphology in broiler chickens supplemented with propolis and bee pollen. Animals 2019;9:301. https://doi.org/10.3390/ani9060301
  128. Hascik P, Trembecka L, Bobko M, Cubon J, Kacaniova M, Tkacova J. Amino acid profile of broiler chickens meat fed diets supplemented with bee pollen and propolis. J Apic Res 2016;55:324-334. https://doi.org/10.1080/00218839.2016.1245398
  129. Kalafova A, Hascik P, Petruska P, et al. Effect of bee poolen in chicken diet on selected parameters of mineral profile. Acta Fytotechn Zootechn 2014;17:90-2. https://doi.org/10.15414/afz.2014.17.03.90-92
  130. Hascik P, Elimam I, Garlik J, et al. Impact of bee pollen as feed supplements on the body weight of broiler Ross 308. Afr J Biotechnol 2012;11:15596-9. https://doi.org/10.5897/AJB12.2239
  131. Acikgoz Z, Yucel B, Altan O. The effects of propolis supplementation on broiler performance and feed digestibility. Eur Poult Sci 2005;69:117-22.
  132. Abdel-Kareem AAA, El-Sheikh TM. Impact of supplementing diets with propolis on productive performance, egg quality traits and some haematological variables of laying hens. J Anim Physiol Anim Nutr 2017;101:441-8. https://doi.org/10.1111/jpn.12407
  133. Rizk YS, Abuoghaba AA, Ismail II, Awadien NB. Egg production, egg quality traits and some hematological parameters of Sinai chicken strain treated with different levels of bee pollen. Egypt Poult Sci 2018;38:427-38.