|Black soldier fly: A new vista for livestock and poultry manure management
ZHANG Ji-bin1, ZHANG Jia1, LI Jia-hui1, Jeffery K. TOMERLIN2, XIAO Xiao-peng1, Kashif ur REHMAN1, 3, CAI Min-min1, ZHENG Long-yu1, YU Zi-niu1
1 State Key Laboratory of Agricultural Microbiology/National Engineering Research Center of Microbial Pesticides/College of Life Science and Technology, Huazhong Agricultural University, Wuhan 430070, P.R.China
2 Department of Entomology, Texas A&M University, TX 77843, USA
3 Livestock and Dairy Development Department, Poultry Research Institute, Rawalpindi 46000, Pakistan
The number of intensive livestock and poultry farms is expected to increase substantially in future because of consumer demand. Unfortunately, such demand also results in a great deal of manure being generated, which threatens the environment if it is not properly managed. Concurrent developments in biotransformation of these wastes with the black soldier fly (BSF), Hermetia illucens (L.) (Diptera: Stratiomydiae), demonstrates such concerns can be abated, while also producing products (e.g., protein, chitin, biodiesel, and fertilizer) of value. In this review, we analyzed the factors influencing black soldier fly larvae (BSFL) conversion processes, the role of microorganisms, and the mechanisms used by BSFL when converting livestock and poultry manure into these valuable products. The effects of BSFL conversion technology on reducing the hazards of such materials and their associated pathogens are reviewed, and the economics of livestock and poultry manure conversion by BSF larvae is discussed.
Received: 18 May 2020
|Fund: This work was supported by the National Key R&D Program of China (2018YFD0500203 and 2018YFF0213503) and the National Natural Science Foundation of China (31770136).
Correspondence ZHANG Ji-bin, Tel: +86-27-87287701, E-mail: email@example.com
Cite this article:
ZHANG Ji-bin, ZHANG Jia, LI Jia-hui, Jeffery K. TOMERLIN, XIAO Xiao-peng, Kashif ur REHMAN, CAI Min-min, ZHENG Long-yu, YU Zi-niu.
Black soldier fly: A new vista for livestock and poultry manure management. Journal of Integrative Agriculture, 20(5): 1167-1178.
| Allegretti G, Talamini E, Schmidt V, Bogorni P C, Ortega E. 2018. Insect as feed: An emergy assessment of insect meal as a sustainable protein source for the Brazilian poultry industry. Journal of Cleaner Product, 171, 403–412.
Alyokhin A, Buzza A, Beaulieu J. 2018. Effects of food substrates and moxidectin on development of black soldier fly, Hermetia illucens. Journal of Applied Entomology, 143, 137–143.
Awasthi M K, Sarsaiya S, Wainaina S, Rajendran K, Kumar S, Quan W, Duan Y M, Awasthi S K, Chen H Y, Pandey A, Zhang Z Q, Jain A, Taherzadeh M J. 2019. A critical review of organic manure biorefinery models toward sustainable circular bioeconomy: Technological challenges, advancements, innovations, and future perspectives. Renewable & Sustainable Energy Reviews, 111, 115–131.
Barraganfonseca 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. Journal of Insects as Food and Feed, 3, 105–120.
Beskin K V, Holcomb C D, Cammack J A, Crippe T L, Knap A H, Sweet S T, Tomberlin J K. 2018. Larval digestion of different manure types by the black soldier fly (Diptera: Stratiomyidae) impacts associated volatile emissions. Waste Management, 74, 213–220.
Bieganowski A, Polakowski C, Wa?ko A, Nowak K, Polak-Berecka M, Bulak P. 2016. The first report of the physicochemical structure of chitin isolated from Hermetia illucens. International Journal of Biological Macromolecules, 92, 316–320.
Bonelli M, Bruno D, Caccia S, Sgambetterra G, Cappellozza S, Jucker C, Tettamanti G, Casartelli M. 2019. Structural and functional characterization of Hermetia illucens larval midgut. Frontiers in Physiology, 10, 204–221.
Bosch G, Felsklerx H, Rijk T, Oonincx D G A B. 2017. Aflatoxin B1 tolerance and accumulation in black soldier fly larvae (Hermetia illucens) and yellow mealworms (Tenebrio molitor). Toxins, 9, 185.
Bruno D, Bonelli M, De Filippis F, Di Lelio I, Tettamanti G, Casartelli M, Ercolini D, Caccia S. 2019. The intestinal microbiota of Hermetia illucens larvae is affected by diet and shows a diverse composition in the different midgut regions. Applied and Environmental Microbiology, 85, 1–14.
Cai M M, Hu R Q, Zhang K, Ma S T. Zheng L Y, Yu Z N, Zhang J B. 2018a. Resistance of black soldier fly (Diptera: Stratiomyidae) larvae to combined heavy metals and potential application in municipal sewage sludge treatment. Environmental Science and Pollution Research, 25, 1559–1567.
Cai M M, Ma S T, Hu R Q, Tomberlin J K, Thomashow L S, Zheng L Y, Li W, Yu Z N, Zhang J B. 2018b. Rapidly mitigating antibiotic resistant risks in chicken manure by Hermetia illucens bioconversion with intestinal microflora. Environmental Microbiology, 20, 4051–4062.
Cai M M, Ma S T, Hu R Q, Tomberlin J K, Yu C, Huang Y P, Zhan S, Li W, Zheng L Y, Yu Z N, Zhang J B. 2018c. Systematic characterization and proposed pathway of tetracycline degradation in solid waste treatment by Hermetia illucens with intestinal microbiota. Environmental Pollution, 242, 634–642.
Chadwick D, Sommer S, Thorman R, Fangueiro D, Cardenas L, Amon B, Misselbrook T. 2011. Manure management: Implications for greenhouse gas emissions. Animal Feed Science and Technology, 166, 514–531.
Chapman R F. 2013. The Insects: Structure and Function. Cambridge University Press, Cambridge, UK.
Chen J S, Hou D J, Pang W C, Nowar E E, Tomberlin J K, Hu R G, Chen H C, Xie J S, Zhang J B, Yu Z N, Li Q. 2019. Effect of moisture content on greenhouse gas and NH3 emissions from pig manure converted by black soldier fly. Science of Total Environment, 697, 133840.
Chen Y B, Li X M, Song J Y, Yang D, Liu W Q, Chen H C, Wu B, Qian P. 2019. Isolation and characterization of a novel temperate bacteriophage from gut?associated Escherichia within black soldier fly larvae (Hermetia illucens L. [Diptera: Stratiomyidae]). Archives of Virology, 164, 2277–2284.
?i?ková H, Newton G L, Lacy R C, Kozánek M. 2015. The use of fly larvae for organic waste treatment. Waste Management, 35, 68–80.
Diener S, Zurbrügg C, Tockner K. 2009. Conversion of organic material by black soldier fly larvae: establishing optimal feeding rates. Waste Management & Research, 27, 603–610.
Elhag O, Zhou D Z, Song Q, Soomro A A, Cai M M, Zheng L L, Yu Z N. Zhang J B. 2017. Screening, expression, purification and functional characterization of novel antimicrobial peptide genes from Hermetia illucens (L.). PLoS ONE, 12, e0169582.
Erickson M C, Islam M, Sheppard C, Liao J, Doyle M P. 2004. Reduction of Escherichia coli O157:H7 and Salmonella enterica serovar Enteritidis in chicken manure by larvae of the black soldier fly. Journal of Food Protection, 67, 685–690.
Fan L X, Yang Z M, Fang Y, Zhang W D. 2019. Utilization status and development suggestion of livestock manure. Modern Agricultural Science and Technology, 1, 175–181. (in Chinese)
Gao Q, Wang X, Wang W, Lei C, Zhu F. 2017. Influences of chromium and cadmium on the development of black soldier fly larvae. Environmental Science and Pollution Research, 24, 8637–8644.
Finley J W. 2020. Evolution and future needs of food chemistry in a changing world. Journal of Agricultural and Food Chemistry, 68, 12956–12971.
Harnden L M, Tomberlin J K. 2016. Effects of temperature and diet on black soldier fly, Hermetia illucens (L.) (Diptera: Stratiomyidae), development. Forensic Science International, 266, 109–166.
Henry M, Gasco L, Piccolo G, Fountoulaki E. 2015. Review on the use of insects in the diet of farmed fish: past and future. Animal Feed Science and Technology, 203, 1–22.
Huang Y Q, Yu Y Q, Zhan S, Tomberlin J K, Huang D, Cai M M, Zheng LY, Yu Z N, Zhang J B. 2020. Dual oxidase Duox and Toll-like receptor 3 TLR3 in the Toll pathway suppress zoonotic pathogens through regulating the intestinal bacterial community homeostasis in Hermetia illucens L. PLoS ONE, 15, e0225873.
Ji Y. 2017. Studies of adaptation to environment complex for Hermetia illucens L. MSc thesis, Guizhou Normal University, China. pp. 15–28. (in Chinese)
Kim J G, Choi Y C, Choi J Y, Kim W T, Jeong G S, Park K H, Hwang S J. 2008. Ecology of the black soldier fly, Hermetia illucens (Diptera; Stratmyidae) in Korea. Korean Journal of Applied Entomology, 47, 337–343.
Kim W, Bae S, Park K, Lee S, Choi Y, Han S, Koh Y. 2011. Biochemical characterization of digestive enzymes in the black soldier fly, Hermetia illucens (Diptera: Stratiomyidae). Journal of Asia-Pacific Entomology, 14, 11–14.
Kong Z J, Wang X Q, Liu Q M, Li T, Chen X, Chai L F, Liu D Y, Shen Q R. 2018. Evolution of various fractions during the windrow composting of chicken manure with rice chaff. Journal of Environmental Management, 207, 366–377.
Lalander C, Diener S, Fidjeland J, Eriksson S, Vinneras B. 2015. High waste-to-biomass conversion and efficient Salmonella spp. reduction using black soldier fly for waste recycling. Agronomy for Sustainable Development, 35, 261–271.
Lalander C, Diener S, Zurbrugg C, Vinneras B. 2019. Effects of feedstock on larval development and process efficiency in waste treatment with black soldier fly (Hermetia illucens). Journal of Cleaner Product, 208, 211–219.
Li L, Stasiak M, Li L, Xie B Z, Fu Y M, Gidzinski D, Dixon M, Liu H. 2016. Rearing Tenebrio molitor in BLSS: Dietary fiber affects larval growth, development, and respiration characteristics. Acta Astronautica, 118, 130–136.
Li Q, Zheng L, Cai H, Garza E, Yu Z, Zhou S. 2011a. From organic waste to biodiesel: Black soldier fly, Hermetia illucens, makes it feasible. Fuel, 90, 1545–1548.
Li Q, Zheng L Y, Qiu N, Cai H, Tomberlin J K, Yu Z N. 2011b. Bioconversion of dairy manure by black soldier fly (Diptera: Stratiomyidae) for biodiesel and sugar production. Waste Management, 31, 1316–1320.
Liu C C, Wang C W, Yao H Y. 2019. Comprehensive resource utilization of waste using the black soldier fly (Hermetia illucens (L.)) (Diptera: Stratiomyidae). Animal, 9, 349.
Liu Q L, Tomberlin J K, Brady J A, Sanford M R, Yu Z N. 2008. Black soldier fly (Diptera: Stratiomyidae) larvae reduce Escherichia coli in dairy manure. Environmental Entomology, 37, 1525–1530.
Liu X, Chen X, Wang H, Yang Q Q, Ur Rehman K, Li W, Cai M M, Li Q, Mazza L, Zhang J B, Yu Z N, Zheng L Y. 2017. Dynamic changes of nutrient composition throughout the entire life cycle of black soldier fly. PLoS ONE, 12, e0182601.
Lohri C R, Diener S, Zabaleta I, Mertenat A, Zurbrügg C. 2017. Treatment technologies for urban solid biowaste to create value products: A review with focus on low- and middle-income settings. Reviews in Environmental Science and Biotechnology, 16, 81–130.
Ma J H, Lei Y Y, Rehman K ur, Yu Z N, Zhang J B, Li W, Li Q, Tomberlin J K, Zheng L Y. 2018. Dynamic effects of initial pH of substrate on biological growth and metamorphosis of black soldier fly (Diptera: Stratiomyidae). Environmental Entomology, 47, 159–165.
Makkar H P S, Tran G, Heuzé V, Ankers P. 2014. State-of-the-art on use of insects as animal feed. Animal Feed Science and Technology, 197, 1–33.
Mazza L, Xiao X P, Rehman K ur, Cai M M, Zhang D N, Fasulo S, Tomberlin J K, Zheng L Y, Soomro A A, Yu Z N, Zhang J B. 2020. Management of chicken manure using black soldier fly (Diptera: Stratiomyidae) larvae assisted by companion bacteria. Waste Management, 102, 312–318.
Meijer N, Stoopen G, van der Fels-Klerx H J, van Loon J J A, Carney J, Bosch G. 2019. Aflatoxin B1 conversion by black soldier fly (Hermetia illucens) larval enzyme extracts. Toxins, 11, 532.
Mekonnen M M, Hoekstra A Y. 2012. A global assessment of the water footprint of farm animal products. Ecosystems, 15, 401–415.
Miglietta P P, De Leo F, Ruberti M, Massari S. 2015. Mealworms for food: A water footprint perspective. Water, 7, 6190–6203.
Miranda C D, Cammack J A, Tomberlin J K. 2019. Life-history traits of the black soldier fly, Hermetia illucens (L.) (Diptera: Stratiomyidae), reared on three manure types. Animals, 9, 1–15.
Myers H M, Tomberlin J K, Lambert B D, Kattes D. 2008. Development of black soldier fly (Diptera: Stratiomyidae) larvae fed dairy manure. Environmental Entomology, 37, 11–15.
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. Animal and Poultry Waste Management Center, North Carolina State University, Raleigh, NC. pp.1– 17.
Nguyen H C, Liang S H, Doan T T, Su C H, Yang P C. 2017, Lipase-catalyzed synthesis of biodiesel from black soldier fly (Hermetica illucens): Optimization by using response surface methodology. Energy Conversion and Management, 145, 335–342.
Nguyen T T X, Tomberlin J K, Vanlaerhoven S. 2013. Influence of resources on Hermetia illucens (Diptera: Stratiomyidae) larval development. Journal of Medical Entomology, 50, 898–906.
Nguyen T T X, Tomberlin J K, Vanlaerhoven S. 2015. Ability of black fly (Diptera: Stratiomyidae) larvae to recycle food waste. Environmental Entomology, 44, 406–410.
Nyakeri E M, Ogola H J, Ayieko M A, Amimo F A. 2017. An open system for farming black soldier fly larvae as a source of proteins for small scale poultry and fish production. Journal of Insects as Food and Feed, 3, 51–56.
Oonincx D G A B, van Huis A, van Loon J J A. 2015. Nutrient utilization by black soldier flies fed with chicken, pig, or cow manure. Journal of Insects as Food and Feed, 1, 131–139.
Park D S, Oh H W, Jeong W J, Kim H, Park H Y, Bae K S. 2007. A culture-based study of the bacterial communities within the guts of nine longicorn beetle species and their exo-enzyme producing properties for degrading xylan and pectin. Journal of Microbiology, 45, 394–401.
Park S I, Kim J W, Yoe S M. 2015. Purification and characterization of a novel antibacterial peptide from black soldier fly (Hermetia illucens) larvae. Developmental and Comparative Immunology, 52, 98–106.
Park S I, Yoe S M. 2017. A novel cecropin-like peptide from black soldier fly, Hermetia illucens: Isolation, structural and functional characterization. Entomological Research, 47, 115–124.
Purschke B, Scheibelberger R, Axmann S, Adler A, Jäger H. 2017. Impact of substrate contamination with mycotoxins, heavy metals and pesticides on growth performance and composition of black soldier fly larvae (Hermetia illucens) for use in the feed and food value chain. Food Additives and Contaminants (Part A: Chemistry Analysis Control Exposure & Risk Assessment), 34, 1410–1420.
Ravindran B, Nguyen D D, Chaudhary D K, Chang S W, Kim J, Lee S R, Shin J, Jeon B H, Chung S, Lee J. 2019. Influence of biochar on physico-chemical and microbial community during swine manure composting process. Journal of Environmental Management, 232, 592–599.
Ur Rehman K, Cai M M, Xiao X P, Zheng L Y, Wang H, Soomro A A, Zhou Y S, Li W, Yu Z N, Zhang J B. 2017a. Cellulose decomposition and larval biomass production from the co-digestion of dairy manure and chicken manure by mini-livestock (Hermetia illucens L.). Journal of Environmental Management, 196, 458–465.
Ur Rehman K, Liu X, Wang H, Zheng L Y, Ur Rehman R, Cheng X, Li Q, Li W, Cai M M, Zhang J B, Yu Z N. 2018. Effects of black soldier fly biodiesel blended with diesel fuel on combustion, performance and emission characteristics of diesel engine. Energy Conversion and Management, 173, 489–498.
Ur Rehman K, Rehman A, Cai M M, Zheng L Y, Xiao X P, Somroo A A, Wang H, Li W, Yu Z N, Zhang J B. 2017b. Conversion of mixtures of dairy manure and soybean curd residue by black soldier fly larvae (Hermetia illucens L.). Journal of Cleaner Product, 154, 366–373.
Ur Rehman K, Ur Rehman R, Somroo A A, Cai M M, Zheng L Y, Xiao X X, Ur Rehman A, Rehman A, Tomberlin J K, Yu Z N, Zhang J B. 2019. Enhanced bioconversion of dairy and chicken manure by the interaction of exogenous bacteria and black soldier fly larvae. Journal of Environmental Management, 237, 75–83.
Roffeis M, Wakefield M E, Almeida J, Alves Valada T R, Devic E, Koné N, Kenis M, Nacambo S, Fitches E C, Koko G K D, Mathijs E, Achten W M J, Muys B. 2018. Life cycle cost assessment of insect based feed production in West Africa. Journal of Cleaner Product, 199, 792–806.
Schiavone A, De Marco M, Martinez S, Dabbou S, Renna M, Madrid J, Hernandez F, Rotolo L, Costa P, Gai F, Gasco L. 2017. 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. Journal of Animal Science and Biotechnology, 8, 51.
Sheppard D C, Newton G L, Thompson S A, Savage S A. 1994. Value added manure management system using the black soldier fly. Bioresource Technology, 50, 275–279.
Sheppard D C, Tomberlin J K, Joyce J A, Kiser B C, Sumner S M. 2002. Rearing methods for the black soldier fly (Diptera: Stratiomyidae). Journal of Medical Entomology, 39, 695–698.
De Smet J, Wynants E, Cos P, Van Campenhout L. 2018. Microbial community dynamics during rearing of black soldier fly larvae (Hermetia illucens) and its impact on exploitation potential. Applied and Environmental Microbiology, 84, e02722–e02739.
St-Hilaire S, Sheppard C, Tomberlin J K, Irving S, Newton L, Mcguire M A, Mosley E E, Hardy R W, Sealey W. 2007. Fly prepupae as a feedstuff for rainbow trout, Oncorhynchus mykiss. Journal of World Aquaculture Society, 38, 59–67.
Thévenot A, Rivera J L, Wilfart A, Maillard F, Hassouna M, Senga-Kiesse T, Le Féon S, Aubin J. 2018. Mealworm meal for animal feed: Environmental assessment and sensitivity analysis to guide future prospects. Journal Cleaner Product, 170, 1260–1267.
Tomberlin J K, Adler P H, Myers H M. 2009. Development of the black soldier fly (Diptera: Stratiomyidae) in relation to temperature. Environmental Entomology, 38, 930–934.
Tomberlin J K, van Huis A. 2020. Black soldier fly from pest to ‘crown jewel’ of the insects as feed industry: An historical perspective. Journal of Insects as Food and Feed, 6, 1–4.
Vogel H, Muller A, Heckel D G, Gutzeit H, Vilcinskas A. 2018. A novel cecropin-like peptide from black soldier fly, Hermetia illucens: Isolation, structural and functional characterization. Developmental and Comparative Immunology, 78, 141–148.
Wang C W, Qian L, Wang W G, Wang T L, Deng Z K, Yang F, Xiong J, Feng W L. 2017. Exploring the potential of lipids from black soldier fly: New paradigm for biodiesel production (I). Renewable Energy, 111, 749–756.
Wang H, Ur Rehman K, Liu X, Yang Q Q, Zheng L Y, Li W, Cai M M, Li Q, Zhang J B, Yu Z N. 2017. Insect biorefinery: A green approach for conversion of crop residues into biodiesel and protein. Biotechnology for Biofuels, 10, 304.
Wang H, Wang S Y, Li H Y, Wang B, Zhou Q S, Zhang X M, Li J, Zhang Z J. 2016. Decomposition and humification of dissolved organic matter in swine manure during housefly larvae composting. Waste Management Research, 34, 465–473.
Wang H R, Ur Rehman K, Feng W J, Yang D, Ur Rehman R, Cai M M, Zhang J B, Yu Z N, Zheng L Y. 2020. Physicochemical structure of chitin in the developing stages of black soldier fly. International Journal of Biological Macromolecules, 149, 901–907.
Warnecke F, Luginbühl P, Ivanova N, Ghassemian M, Richardson T H, Stege J T, Cayouette M, McHardy A C, Djordjevic G, Aboushadi N, Sorek R, Tringe S G, Podar M, Martin H G, Kunin V, Dalevi D, Madejska J, Kirton E, Platt D, Szeto E, et al. 2007. Metagenomic and functional analysis of hindgut microbiota of a wood-feeding higher termite. Nature, 450, 560–565.
Wu N, Wang X B, Xu X Y, Cai R J, Xie S Y. 2020. Effects of heavy metals on the bioaccumulation, excretion and gut microbiome of black soldier fly larvae (Hermetia illucens). Ecotoxicology and Environmental Safety, 192, 1–8.
Xiao X P, Jin P, Cai M M, Zheng L Y, Li W, Yu Z N, Zhang J B. 2018a. Chicken manure co-conversion by Hermetia illucens larvae with non-associated microorganism. Acta Microbiologica Sinica, 56, 1116–1125. (in Chinese)
Xiao X P, Mazza L, Yu Y Q, Cai M M, Zheng L Y, Tomberlin J K, Yu J, van Huis A, Yu Z N, Fasulo S, Zhang J. 2018b. Efficient co-conversion process of chicken manure into protein feed and organic fertilizer by Hermetia illucens L. (Diptera: Stratiomyidae) larvae and functional bacteria. Journal of Environmental Management, 217, 668–676.
Yang S. 2010. Continuous culture of Hermrtia illucens L. and study on swine manure bioconversion tropical region. MSc thesis, Huazhong Agricultural University, China. pp. 18–24. (in Chinese)
Yu G H, Cheng P, Chen Y H, Li Y J, Yang Z H, Chen Y F, Tomberlin J K. 2011. Inoculating poultry manure with companion bacteria influences growth and development of black soldier fly (Diptera: Stratiomyidae) larvae. Environmental Entomology, 40, 30–35.
Zhan S, Fang G Q, Cai M M, Kou Z Q, Xu J, Cao Y H, Bai L, Zhang Y X, Jiang Y M, Luo X Y, Xu J, Xu X, Zheng L Y, Yu Z N, Yang H, Zhang Z J, Wang S B, Tomberlin J K, Zhang J B, Huang Y P. 2020. Genomic landscape and genetic manipulation of the black soldier fly Hermetia illucens, a natural waste recycler. Cell Research, 30, 50–60.
Zhang J B, Tomberlin J K, Cai M M, Xiao X P, Zheng L Y, Yu Z N. 2020. Research and industrialization of Hermetia illucens L. in China. Journal of Insects as Food and Feed, 6, 5–12.
Zhang Z J, Wang H, Zhu J, Suneethi S, Zheng J G. 2012. Swine manure vermicomposting via housefly larvae (Musca domestica): The dynamics of biochemical and microbial features. Bioresource Technology, 118, 563–571.
Zheng L Y, Hou Y F, Li W, Yang S, Li Q, Yu Z. 2012. Biodiesel production from rice straw and restaurant waste employing black soldier fly assisted by microbes. Energy, 47, 22–229.
Zhou F, Tomberlin J K, Zheng L Y, Yu Z N, Zhang J B. 2013. Developmental and waste reduction plasticity of three black soldier fly strains (Diptera: Stratiomyidae) raised on different livestock manures. Journal of Medical Entomology, 50, 1224–1230.
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