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Nutritional composition of various insects and potential uses as alternative protein sources in animal diets

  • Shah, Assar Ali (Tropical Feed Resources Research and Development Center (TROFREC), Department of Animal Science, Faculty of Agriculture, Khon Kaen University) ;
  • Totakul, Pajaree (Tropical Feed Resources Research and Development Center (TROFREC), Department of Animal Science, Faculty of Agriculture, Khon Kaen University) ;
  • Matra, Maharach (Tropical Feed Resources Research and Development Center (TROFREC), Department of Animal Science, Faculty of Agriculture, Khon Kaen University) ;
  • Cherdthong, Anusorn (Tropical Feed Resources Research and Development Center (TROFREC), Department of Animal Science, Faculty of Agriculture, Khon Kaen University) ;
  • Hanboonsong, Yupa (Department of Entomology and Plant Pathology, Faculty of Agriculture, Khon Kaen University) ;
  • Wanapat, Metha (Tropical Feed Resources Research and Development Center (TROFREC), Department of Animal Science, Faculty of Agriculture, Khon Kaen University)
  • Received : 2021.10.05
  • Accepted : 2021.11.22
  • Published : 2022.02.01

Abstract

The aim of the present investigation is to determine the nutritional composition of various insects and their potential uses as alternative protein sources in animal diets. The feeding industry requires production systems that use accessible resources, such as feed resources, and concentrates on the potential impacts on production yield and nutritional quality. Invertebrate insects, such as black soldier flies, grasshoppers, mealworms, housefly larvae, and crickets, have been used as human food and as feed for nonruminants and aqua culture while for ruminants their use has been limited. Insects can be mass-produced, participating in a circular economy that minimizes or eliminates food- and feed-waste through bioconversion. Although the model for formula-scale production of insects as feed for domestic animals has been explored for a number of years, significant production and transformation to being a conventional protein resource remains to be deeply investigated. This review will focus on the nutritional composition of various insects and their potential use as alternative protein sources, as well as their potential use to promote and support sustainable animal production. Furthermore, nutritional compositions, such as high protein, lauric acid omega 6, and omega 3, and bioactive compounds, such as chitin, are of great potential use for animal feeding.

Keywords

Acknowledgement

Thanks are extended to the Postdoctoral Fellowship of KKU 2021, supporting the first author and National Research Council of Thailand (NRCT) through the Basic Research Fund (record no. 2564A10302002). Special thanks to Professor Y. Hanboonsong for her advice and the video presentation. Sincere gratitudes are extended to TROFREC, Department of Animal Science, Faculty of Agriculture, Khon Kaen University, Thailand.

References

  1. Da-Silva Lucas AJ, de Oliveira LM, da Rocha M, Prentice C. Edible insects: An alternative of nutritional, functional and bioactive compounds. Food Chemist 2020;311:126022. https://doi.org/10.1016/j.foodchem.2019.126022
  2. Makkar HPS. Review: Feed demand landscape and implications of food-not feed strategy for food security and climate change. Animal 2018;12:1744-54. https://doi.org/10.1017/S175173111700324X
  3. Meneguz M, Schiavone A, Gai F, et al. Effect of rearing substrate on growth performance, waste reduction efficiency and chemical composition of black soldier fly (Hermetia illucens) larvae. J Sci Food Agric 2018;98:5776-84. https://doi.org/10.1002/jsfa.9127
  4. FAO. The State of Food and Agriculture: Livestock in the Balance. Rome, Italy: Food and Agriculture Organization of the United Nations; 2009.
  5. 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
  6. Hussein M, Pillai VV, Goddard JM, et al. Sustainable production of housefly (Musca domestica) larvae as a protein-rich feed ingredient by utilizing cattle manure. PLoS ONE 2017; 12: e0171708. https://doi.org/10.1371/journal.pone.0171708
  7. Miech P, Lindberg JE, Berggren A, Chhay T, Jansson A. Apparent faecal digestibility and nitrogen retention in piglets fed whole and peeled Cambodian field cricket meal. J Insect Food Feed 2017;3:279-88. https://doi.org/10.3920/JIFF2017.0019
  8. 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
  9. 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;12:2032-9. https://doi.org/10.1017/S1751731117003743
  10. Secci G, Moniello G, Gasco L, Bovera F, Parisi G. Barbary partridge meat quality as affected by Hermetia illucens and Tenebrio molitor larva meals in feeds. Food Res Int 2018;112: 291-8. https://doi.org/10.1016/j.foodres.2018.06.045
  11. Gasco L, Finke M, van Huis A. Can diets containing insects promote animal health? J Insect Food Feed 2018;4:1-4. https://doi.org/10.3920/JIFF2018.x001
  12. Onsongo VOI, 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;111:1966-73. https://doi.org/10.1093/jee/toy118
  13. Sealey WM, Gaylord TG, Barrows FT, et al. Sensory Analysis of Rainbow Trout, Oncorhynchus mykiss, Fed Enriched Black Soldier Fly Prepupae, Hermetia illucens. J World Aquac Soc 2011;42:34-45. https://doi.org/10.1111/j.1749-7345.2010.00441.x
  14. Barroso FG, de Haro C, Sanchez-Muros MJ, Venegas E, Martinez-Sanchez A, Perez-Banon C. The potential of various insect species for use as food for fish. Aquaculture 2014;422: 193-201. https://doi.org/10.1016/j.aquaculture.2013.12.024
  15. Van Huis A. Potential of insects as food and feed in assuring food security. Annu Rev Entomol 2013;58:563-83. https://doi.org/10.1146/annurev-ento-120811-153704
  16. Ahmed S, Al Baki MA, Lee J, Seo DY, Lee D, Kim Y. The first report of prostacyclin and its physiological roles in insects. Gen Comp Endocrinol 2021;301:113659. https://doi.org/10.1016/j.ygcen.2020.113659
  17. Khusro M, Andrew NR, Nicholas A. Insects as poultry feed: a scoping study for poultry production systems in Australia. World's Poult Sci J 2012;68:435-46. https://doi.org/10.1017/S0043933912000554
  18. Zhang L, Lecoq M, Latchininsky A, Hunter D. Locust and grasshopper management. Annu Rev Entomol 2019;64:1534. https://doi.org/10.1146/annurev-ento-011118-112500
  19. Ojewola GS, Eburuaja AS, Okoye FC, Lawal AS, Akinmutimi AH. Effect of inclusion of grasshopper meal on performance nutrient utilization and organ of broiler chicken. J Sustain Agric Environ 2003;5:19-25.
  20. Wang D, Zhai SW, Zhang CX, Zhang Q, Chena 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
  21. Ghosh S, Parimalendu H, Dipak KM. 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.
  22. Ssepuuya G, Mukisa IM, Nakimbugwe D. Nutritional composition, quality, and shelf stability of processed Ruspolia nitidula (edible grasshoppers). Food Sci Nutr 2017;5:103-12. https://doi.org/10.1002/fsn3.369
  23. Straub P, Tanga CM, Osuga I, Windisch W, Subramanian S. Experimental feeding studies with crickets and locusts on the use of feed mixtures composed of storable feed materials commonly used in livestock production. Anim Feed Sci Technol 2019;255:114215. https://doi.org/10.1016/j.anifeedsci.2019.114215
  24. Patton RS, Chandler PT. In vivo digestibility evaluation of chitinous materials. J Dairy Sci 1975;58:397-403. https://doi.org/10.3168/jds.S0022-0302(75)84577-2
  25. Kinyuru JN, Kenji GM, Njoroge SM, Ayieko M. Effect of processing methods on the in vitro protein digestibility and vitamin content of edible winged termite (Macrotermes subhylanus) and grasshopper (Ruspolia differens). Food Bioproc Tech 2010;3:778-82. https://doi.org/10.1007/s11947009-0264-1
  26. Opstvedt J, Nygard E, Samuelsen TA, Venturini G, Luzzana U, Mundheim H. Effect on protein digestibility of different processing conditions in the production of fish mealand fish feed. J Sci Food Agric 2003;83:775-82. https://doi.org/10.1002/jsfa.1396
  27. Nafisa ME, Hassan SY, Hamed AB, Hassan MM, Elfadil EB. Nutritional evaluation and physiochemical properties of boiled and fried tree locust. Pakistan J Nutr 2008;7:325-9. https://doi.org/10.3923/pjn.2008.325.329
  28. Nginya ES, Ondiek JO, King'ori AM, Nduko JM. Evaluation of grasshoppers as a protein source for improved indigenous chicken growers. Breas 2019;62:1-45. http://www.lrrd.org/lrrd31/1/shilo31002.html
  29. Moula N, Detilleux J. A meta-analysis of the effects of insects in feed on poultry growth performances. Animals 2019;9:201. https://doi.org/10.3390/ani9050201
  30. Brah N, Houndonougbo FM, Issa S. Grasshopper meal (Ornithacris cavroisi) in broiler diets in Niger: Bioeconomic performance. Int J Poult Sci 2018;17:126-33. https://doi.org/10.3923/ijps.2018.126.133
  31. Falade KO, Omojola BS. Effect of Processing Methods on physical, chemical, rheological, and sensory properties of Okra (Abelmoschus esculentus). Food Bioproc Technol 2010;3:387-94. https://doi.org/10.1007/s11947-008-0126-2
  32. Patterson PH, Acar N, Ferguson AD, Trimble LD, Sciubba HB, Koutsos EA. The impact of dietary Black Soldier Fly larvae oil and meal on laying hen performance and egg quality. Poult Sci 2021;100:101272. https://doi.org/10.1016/j.psj.2021.101272
  33. Arango Gutierrez GP, Vergara Ruiz RA, Mejia Velez H. Compositional microbiological and protein digestibility analysis of larval meal of Hermetia illucens (Diptera:Stratiomyidae) at Angelopolis-Antioquia Colombia. Rev Fac Nac Agron Medellin 2004;57:2491-9.
  34. St-Hilaire S, Sheppard C, Tomberlin JK, et al. Fly prepupae as a feedstuff for rainbow trout Oncorhynchus mykiss. J World Aquac Soc 2007;38:59-67. https://doi.org/10.1111/j.1749-7345.2006.00073.x
  35. Cullere M, Tasoniero G, Giaccone V, et al. Black soldier fly as dietary protein source for broiler quails: apparent digestibility, excreta microbial load, feed choice, performance, carcass and meat traits. Animal 2016;10:1923-30. https://doi.org/10.1017/S1751731116001270
  36. 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;209:211-8. https://doi.org/10.1016/j.anifeedsci.2015.08.006
  37. Jayanegara A, Yantina N, Novandri B, Laconi EB, Nahrowi N, Ridla M. Evaluation of some insects as potential feed ingredients for ruminants: chemical composition, in vitro rumen fermentation and methane emissions. J Indones Trop Anim Agric 2017;42:247-54. https://doi.org/10.14710/jitaa.42.4.247254
  38. Owens FN, Qi S, Sapienza AD. Applied protein nutrition of ruminants current status and future directions. Anim Sci 2014;30:150-79. https://doi.org/10.15232/S1080-7446(15)30102-9
  39. Jayanegara A, Dewi SP, Ridla M. Nutrient Content, Protein Fractionation, and Utilization of Some Beans as Potential Alternatives to Soybean for Ruminant Feeding. Med Pet 2016; 39:195-202. https://doi.org/10.5398/medpet.2016.39.3.195
  40. Jayanegara AG, Goel HP, Makkar S, Becker K. Divergence between purified hydrolysable and condensed tannin effects on methane emission rumen fermentation and microbial population in vitro. Anim Feed Sci Technol 2015;209:60-8. https://doi.org/10.1016/j.anifeedsci.2015.08.002
  41. Boushy AR. House-fly pupae as poultry manure converters for animal feed: a review. Bioresour Technol 1991;38:45-9. https://doi.org/10.1016/0960-8524(91)90220-E
  42. Campbell M, Ortuno J, Stratakos AC, et al. Impact of thermal and high-pressure treatments on the microbiological quality and in vitro digestibility of black soldier fly (Hermetia illucens) Larvae. Animal 2020;10:682. https://doi.org/10.3390/ani10040682
  43. Moreki JC, Tiroesele B, Chiripasi SC. Prospects of utilizing insects as alternative sources of protein in poultry diets in Botswana. J Anim Sci Adv 2012;2:649-58.
  44. 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.
  45. Bosch G, Zhang S, Oonincx DGAB, Hendriks WH. Protein quality of insects as potential ingredients for dog and cat foods. J Nutr Sci 2014;3:E29. https://doi.org/10.1017/jns.2014.23
  46. Ukanwoko AI, Olalekan OA. Effects of source and time of harvest on the proximate composition of maggot (Musca Domestica) larva meal. Int J Livest Res 2015;5:84-90. https://doi.org/10.5455/ijlr.20150713102839
  47. Pieterse E, Pretorius Q. Nutritional evaluation of dried larvae and pupae meal of the housefly (Musca domestica) using chemical- and broiler-based biological assays. Anim Prod Sci 2013;54:347-55. https://doi.org/10.1071/AN12370
  48. Rumpold BA, Oliver KS. Potential and challenges of insects as an innovative source for food and feed production. Innov Food Sci Emerg Technol 2013;17:1-11. https://doi.org/10.1016/j.ifset.2012.11.005
  49. 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
  50. Jozefiak D, Jozefiak A, Kieronczyk B, et al. Insects a natural nutrient source for poultry a review. Ann Anim Sci 2016; 16:297-313. https://doi.org/10.1515/aoas-2016-0010
  51. Ravzanaadii N, Kim SH, Choi WH, Hong SJ, Kim NJ. Nutritional value of mealworm, Tenebrio molitor as food source. Int J Indust Entomol 2012;25:93-8. https://doi.org/10.7852/ijie.2012.25.1.093
  52. Shah AA, Liu Z, Qian C, Wu J, Sultana N, Zhong X. Potential effect of the microbial fermented feed utilization on physicochemical traits, antioxidant enzyme and trace mineral analysis in rabbit meat. J Anim Physiol Anim Nutr 2020;104: 767-75. https://doi.org/10.1111/jpn.13252
  53. Gasco L, Dabbou S, Trocino A, et al. Effect of dietary supplementation with insect fats on growth performance, digestive efficiency and health of rabbits. J Anim Sci Biotechnol 2019; 10:4. https://doi.org/10.1186/s40104-018-0309-2
  54. Gugolek A, Strychalski J, Juskiewicz J, Zary-Sikorska E. The effect of fish and mealworm larvae meals as alternative dietary protein sources on nutrient digestibility and gastro-intestinal function in Chinchilla lanigera. Exp Anim 2020; 69:70-9. https:// doi.org/10.1538/expanim.19-0072
  55. Marono S, Piccolo G, Loponte R, et al. In vitro crude protein digestibility of tenebrio molitor and hermetia illucens insect meals and its correlation with chemical composition traits. Ital J Anim Sci 2015;14:3389. https://doi.org/10.4081/ijas.2015.3889
  56. Song YS, Kim MW, Moon C, et al. Extraction of chitin and chitosan from larval exuvium and whole body of edible mealworm, Tenebrio molitor. Entomol Res 2018;48:227-33. https://doi.org/10.1111/1748-5967.12304
  57. Matin N, Utterback P, Parsons CM. True metabolizable energy and amino acid digestibility in black soldier fly larvae meals, cricket meal, and mealworms using a precision-fed rooster assay. Poult Sci 2021;100:101146. https://doi.org/10.1016/j.psj.2021.101146
  58. Yoo JS, Cho KH, Hong JS, et al. Nutrient ileal digestibility evaluation of dried mealworm (Tenebrio molitor) larvae compared to three animal protein by-products in growing pigs. Asian-Australas J Anim Sci 2019;32:387-94. https://doi.org/10.5713/ajas.18.0647
  59. Schiavone A, De Marco M, Rotolo L, et al. Nutrient digestibility of Hermetia illucens and Tenebrio molitor meal in broiler chickens. In: Abstract book Conference "Insects to Feed the World" 2014 May 14-17 Wageningen The Netherlands. 84 p. https://iris.unito.it/handle/2318/158360#.YQS1AUBRXIU
  60. Jin XH, Heo PS, Hong JS, Kim NJ, Kim YY. Supplementation of dried mealworm (Tenebrio molitor larva) on growth performance, nutrient digestibility and blood profiles in weaning pigs. Asian-Australas J Anim Sci 2016;29:979-86. https://doi.org/10.5713/ajas.15.0535
  61. Stein HH, Kim SW, Nielsen TT. Standardized ileal protein and amino acid digestibility by growing pigs and sows. J Anim Sci 2001;79:2113-22. https://doi.org/10.2527/2001.7982113x
  62. Veldkamp T, Bosch G. Insects: a protein-rich feed ingredient in pig and poultry diets. Anim Front 2015;5:45-50.
  63. Veldkamp T, Van Duinkerken G, van Huis A, et al. Insects as a sustainable feed ingredient in pig and poultry diets: a feasibility study Insecten als duurzame diervoedergrondstof in varkens-en pluimveevoeders: eenhaalbaarheidsstudie (No 638). Wageningen, The Nederlands: Wageningen University Research Livestock Research; 2012.
  64. Malla N, Opeyemi AJ. Prospects of insects as alternative protein source: broiler chicken and growing pigs. Report in Sustainable Animal Nutrition and Feeding. Aarhus, Denmark: Department of Animal Science, Aarhus University; 2018. 26 p.
  65. Cickova H, Newton GL, Lacy RC, Kozanek M. The use of fly larvae for organic waste treatment. J Waste Manag 2015;35: 68-80. https://doi.org/10.1016/j.wasman.2014.09.026
  66. 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
  67. Madau FA, Arru B, Furesi R, Pulina P. Insect farming for feed and food production from a circular business model perspective. Sustainability 2020;12:5418. https://doi.org/10.3390/su12135418
  68. Yen AL. Insects as food and feed in the Asia Pacific region: Current perspectives and future directions. J Insects Food Feed 2015;1:33-55. https://doi.org/10.3920/JIFF2014.0017
  69. Oonincx DGAB, de Boer IJM. Environmental impact of the production of mealworms as a protein source for humans a life cycle assessment. PLoS ONE 2012;7:e51145. https:// doi.org/10.1371/journal.pone.0051145
  70. Van Huis A, Oonincx DGAB. The environmental sustainability of insects as food and feed. A review. Agron Sustain Dev 2017;37:43. https://doi.org/10.1007/s13593-017-0452-8
  71. Mlcek J, Rop O, Borkovcova M, Bednarova MA. A Comprehensive look at the possibilities of edible insects as food in Europe a review. Pol J Food Nutr Sci 2014;64:147-57. https://doi.org/10.2478/v10222-012-0099-8
  72. Govorushko S. Global status of insects as food and feed source: a review. Trends Food Sci Technol 2019;91:436-45. https://doi.org/10.1016/j.tifs.2019.07.032
  73. Kim TK, Yong HI, Kim YB, Kim HW, Choi YS. Edible insects as a protein source: a review of public perception, processing technology, and research trends. Food Sci Anim Resour 2019; 39:521-40. https://doi.org/10.5851/kosfa.2019.e53
  74. Derrien C, Boccuni A. Current status of the insect producing industry in Europe. In: Halloran A, Flore R, Vantomme P, Roos N, editors. Edible insects in sustainable food systems. Berlin/Heidelberg Germany: Springer; 2018. pp. 471-9. https://doi.org/10.1007/978-3-319-74011-9_30
  75. Diener S, Solano NMS, Gutierrez FR, Zurbrugg C, Tockner K. Biological treatment of municipal organic waste using black soldier fly larvae. Waste Biomass Valorization 2011;2: 357-63. https://doi.org/10.1007/s12649-011-9079-1
  76. Mordor Intelligence Insect Feed Market Growth Trends and Forecasts (2020-2025) 2019 [cited 2020 June 30]. Available from: https://wwwmordorintelligencecom/industry-reports/insect-feed-market
  77. Gahukar RT. Edible insects farming: efficiency and impact on family livelihood, food security, and environment compared with livestock and crops. In: Dossey AT, Morales-Ramos JA, Rojas MG, editors. Insects as sustainable food ingredients. Academic Press; 2016. pp. 85-111. https://doi.org/10.1016/B978-0-12-802856-8.00004-1
  78. Arru B, Furesi R, Gasco L, Madau FA, Pulina P. The introduction of insect meal into fish diet: the first economic analysis on European sea bass farming. Sustainability 2019;11:1697. https://doi.org/10.3390/su11061697
  79. Imathiu S. Benefits and food safety concerns associated with consumption of edible insects. NFS J 2020;18:1-11. https://doi.org/10.1016/j.nfs.2019.11.002
  80. Lahteenmaki-Uutela A, Marimuthu SB, Meijer N. Regulations on insects as food and feed: a global comparison. J Insects Food Feed 2021;7:849-56. https://doi.org/10.3920/JIFF2020.0066
  81. Hanboonsong Y, Jamjanya T, Durst PB. Six-legged livestock: edible insect farming, collecting and marketing in Thailand. Food and Agriculture Organization of the United Nations; 2013. Bangkok, 1-69. http://www.fao.org/3/i3246e/i3246e.pdf
  82. IPIFF (International Platform Insects for Food & Feed) EU Legislation [cited 2017 Sept 8]. Available from: www.ipiff. org/our-positions
  83. Halloran A, Vantomme P, Hanboonsong Y, Ekesi S. Regulating edible insects: the challenge of addressing food security, nature conservation, and the erosion of traditional food culture. Food Secur 2015;7:739-46. https://doi.org/10.1007/s12571-015-0463-8
  84. Preteseille N, Deguerry A, Reverberi M, Weigel T. Insects in Thailand: national leadership and regional development, from standards to regulations through association. In: Halloran A, Flore R, Vantomme P, Roos N, editors. Edible insects in sustainable food systems. Berlin/Heidelberg Germany: Springer; 2018. pp. 435-42. https://doi.org/10.1007/978-3319-74011-9_27
  85. Feng Y, Chen XM, Zhao M, et al. Edible insects in China: Utilization and prospects. Insect Sci 2018;25:184-98. https://doi.org/10.1111/1744-7917.12449