Growth performance and nutrient composition of black soldier fly larvae reared on solid-state fermentation substrates with various white rot fungi

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EKO LELA FITRIANA
https://orcid.org/0000-0002-9716-4591
ANURAGA JAYANEGARA
https://orcid.org/0000-0001-7529-9770
DEWI APRI ASTUTI
https://orcid.org/0000-0001-8655-9304
ERIKA BUDIARTI LACONI
https://orcid.org/0000-0001-9213-488X

Abstract

Abstract. Fitriana EL, Jayanegara A, Astuti DA, Laconi EB. 2022. Growth performance and nutrient composition of black soldier fly larvae reared on solid-state fermentation substrates with various white rot fungi. Biodiversitas 23: 4894-4905. This study examines agricultural byproducts fermented with various rot fungi as a substrate of black soldier fly larvae. The experiment used a three-way randomized design with four replications. The first factor was substrate (cacao pod husk and oil palm frond), the second factor was fungi (Phanerochaete chrysosporium, Trametes versicolor, and Pleurotus sajor-caju), and the third factor was environment condition (light and without light). Approximately 1200 of 7-day-old larvae were added to 600 g substrate treatment. The results showed that the solid-state fermentation substrates had the highest waste reduction parameters and level of consumption. Larvae in the experiment had a crude protein level of 38.84-58.88% of dry matter. Glutamic acid is the most abundant non-essential amino acid in larvae, while leucine is the most abundant essential amino acid. Solid-state fermentation substrate could improve the fatty acid profile quality of larvae in relation to high linoleic acid, polyunsaturated fatty acid, and unsaturated fatty acid percentages, especially CPH-pc substrate. The use of solid-state fermentation in larvae rearing decreased lignin in the cacao pod husk substrate. In conclusion, cacao pod husk substrate solid-state fermented with white rot fungi is not supported the optimum growth performance of BSFL but increases fatty acid profile quality.

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References
Adebayo HA, Kemabonta KA, Ogbogu SS, Elechi MC, Obe MT. 2021. Comparative assessment of developmental parameters, proximate analysis, and mineral compositions of black soldier fly (Hermetia illucens) prepupae reared on organic waste substrates. Int J Trop Insect Sci 2:1-7. DOI: 10.1007/s42690-020-00404-4.
Association of Official Analytical Chemists. 2005. Official methods of analysis, AOAC International, Washington DC, USA.
Barragan-Fonseca KB, Dicke M, Loon JJA van. 2018. Influence of larval density and dietary nutrient concentration on performance, body protein, and fat contents of black soldier fly larvae (Hermetia illucens). Entomol Exp Appl 166:761–770. DOI: 10.1111/eea.12716.
Bejaei M, Cheng KM. 2020. The effect of including full-fat dried black soldier fly larvae in laying hen diet on egg quality and sensory characteristics. J Insects as Food Feed 6:305–314. DOI: 10.3920/JIFF2019.0045.
Biasato I, Ferrocino I, Dabbou S, Evangelista R, Gai F, Gasco L, Cocolin L, Capucchio MT, Schiavone A. 2020. Black soldier fly and gut health in broiler chickens: Insights into the relationship between cecal microbiota and intestinal mucin composition. J Anim Sci Biotechnol 11:1–12. DOI: 10.1186/s40104-019-0413-y.
Bonelli M, Bruno D, Brilli M, Gianfranceschi N, Tian L, Tettamanti G, Caccia S, Casartelli M. 2020. Black soldier fly larvae adapt to different food substrates through morphological and functional responses of the midgut. Int J Mol Sci 21:1–27. DOI: 10.3390/ijms21144955.
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. Appl Environ Microbiol 85:1–14. DOI: 10.1128/AEM.01864-18.
Chia SY, Tanga CM, Osuga IM, Cheseto X, Ekesi S, Dicke M, van Loon JJA. 2020. Nutritional composition of black soldier fly larvae feeding on agro-industrial by-products. Entomol Exp Appl 168:472–481. DOI: 10.1111/eea.12940.
Cullere M, Schiavone A, Dabbou S, Gasco L, Zotte AD. 2019. Meat quality and sensory traits of finisher broiler chickens fed with black soldier fly (Hermetia illucens L.) larvae fat as alternative fat source. Animals 9:1–15. DOI: 10.3390/ani9040140.
Diener S, Zurbrügg C, Tockner K. 2009. Conversion of organic material by black soldier fly larvae: Establishing optimal feeding rates. Waste Manag Res 27:603–610. DOI: 10.1177/0734242X09103838.
Dietrich C, Köhler T, Brune A. 2014. The cockroach origin of the termite gut microbiota: Patterns in bacterial community structure reflect major evolutionary events. Appl Environ Microbiol 80:2261–2269. DOI: 10.1128/AEM.04206-13.
Do S, Koutsos L, Utterback PL, Parsons CM, De Godoy MRC, Swanson KS. 2020. Nutrient and AA digestibility of black soldier fly larvae differing in age using the precision-fed cecectomized rooster assay. J Anim Sci 98:skz363. DOI: 10.1093/jas/skz363.
Ewald N, Vidakovic A, Langeland M, Kiessling A, Sampels S, Lalander C. 2020. Fatty acid composition of black soldier fly larvae (Hermetia illucens) – possibilities and limitations for modification through diet. Waste Manag 102:40–47. DOI: 10.1016/j.wasman.2019.10.014.
Fischer H, Romano N, Sinha AK, 2021. Conversion of spent coffee and donuts by black soldier fly (Hermetia illucens) larvae into potential resources for animal and plant farming. Insects 12:332. DOI: 10.3390/insects12040332.
Gao Z, Wang W, Lu X, Zhu F, Liu W, Wang X, Lei C. 2019. Bioconversion performance and life table of black soldier fly (Hermetia illucens) on fermented maize straw. J Clean Prod 230:974–980. DOI: 10.1016/j.jclepro.2019.05.074.
Giannetto A, Oliva S, Ceccon Lanes CF, de Araújo Pedron F, Savastano D, Baviera C, Parrino V, Lo Paro G, Spanò NC, Cappello T, Maisano M, Mauceri A, Fasulo S. 2020. Hermetia illucens (Diptera: Stratiomydae) larvae and prepupae: Biomass production, fatty acid profile and expression of key genes involved in lipid metabolism. J Biotechnol 307:44–54. DOI: 10.1016/j.jbiotec.2019.10.015.
Gold M, Tomberlin JK, Diener S, Zurbrügg C, Mathys A. 2018. Decomposition of biowaste macronutrients, microbes, and chemicals in black soldier fly larval treatment: a review. Waste Manag 82:302–318. DOI: 10.1016/j.wasman.2018.10.022.
Hoc B, Genva M, Fauconnier ML, Lognay G, Francis F, Caparros Megido R. 2020. About lipid metabolism in Hermetia illucens (L. 1758): On the origin of fatty acids in prepupae. Sci Rep 10:1–8. DOI: 10.1038/s41598-020-68784-8.
Howdeshell T, Tanaka T. 2018. Recovery of glucose from dried distiller’s grain with solubles, using combinations of solid-state fermentation and insect culture. Can J Microbiol 64:706–715. DOI: 10.1139/cjm-2018-0042.
Jayanegara A, Novandri B, Yantina N, Ridla M. 2017. Use of black soldier fly larvae (Hermetia illucens) to substitute soybean meal in ruminant diet: An in vitro rumen fermentation study. Vet World 10:1439–1446. DOI: 10.14202/vetworld.2017.1439-1446.
Jiang CL, Jin WZ, Tao XH, Zhang Q, Zhu J, Feng SY, Xu XH, Li HY, Wang ZH, Zhang ZJ. 2019. Black soldier fly larvae (Hermetia illucens) strengthen the metabolic function of food waste biodegradation by gut microbiome. Microb Biotechnol 12:528–543. DOI: 10.1111/1751-7915.13393.
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). J Asia Pac Entomol 14:11–14. DOI: 10.1016/j.aspen.2010.11.003.
Kim YB, Kim DH, Jeong SB, Lee JW, Kim TH, Lee, HG, Lee KW. 2020. Black soldier fly larvae oil as an alternative fat source in broiler nutrition. Poult Sci 99:3133–3143. DOI: 10.1016/j.psj.2020.01.018.
Klammsteiner T, Walter A, Bogataj T, Heussler CD, Stres B, Steiner FM, Schlick-Steiner BC, Arthofer W, Insam H. 2020. The core gut microbiome of black soldier fly (Hermetia illucens) larvae raised on low-bioburden diets. Front Microbiol 11:993. DOI: 10.3389/fmicb.2020.00993.
Klüber P, Bakonyi D, Zorn H, Rühl M. 2020. Does light color temperature influence aspects of oviposition by the black soldier fly (Diptera: Stratiomyidae)? J Econ Entomol 113:2549–2552. https://doi.org/10.1093/jee/toaa182.
Kumneadklang S, O-Thong S, Larpkiattaworn S. 2019. Characterization of cellulose fiber isolated from oil palm frond biomass. Mater Today Proc 17:1995–2001. DOI: 10.1016/j.matpr.2019.06.247.
Kuttiyatveetil JRA, Mitra P, Goldin D, Nickerson MT, Tanaka T. 2019. Recovery of residual nutrients from agri-food by-products using a combination of solid-state fermentation and insect rearing. Int J Food Sci Technol 54:1130–1140. DOI: 10.1111/ijfs.14015.
Lalander C, Diener S, Zurbrügg C, Vinnerås B. 2019. Effects of feedstock on larval development and process efficiency in waste treatment with black soldier fly (Hermetia illucens). J Clean Prod 208:211–219. DOI: 10.1016/j.jclepro.2018.10.017.
Lee C, Lee Y, Seo S, Yoon S, Kim S, Hahn B, Sim J, Koo B. 2014. Screening and characterization of a novel cellulase gene from the gut microflora of Hermetia illucens using metagenomic library. J Microbiol Biotechnol 24:1196–1206. DOI: 10.4014/jmb.1405.05001.
Manurung R, Supriatna A, Esyanthi RR. 2016. Bioconversion of rice straw waste by black soldier fly larvae (Hermetia illucens L.): Optimal feed rate for biomass production. J Entomol Zool Stud 4:1036–1041.
Marusich E, Mohamed H, Afanasiev Y, Leonov S. 2020. Fatty acids from Hermetia illucens larvae fat inhibit the proliferation and growth of actual phytopathogens. Microorganisms 8:1–21. DOI: 10.3390/microorganisms8091423.
Meneguz M, Schiavone A, Gai F, Dama A, Lussiana C, Renna M, Gasco L. 2018. Effect of rearing substrate on growth performance, waste reduction efficiency and chemical composition of black soldier fly (Hermetia illucens) larvae. J Sci Food Agric 98:5776–5784. DOI: 10.1002/jsfa.9127.
Miner LP, Fernandez-Bayo J, Putri F, Niemeier D, Bischel H, VanderGheynst JS. 2022. Predicting black soldier fly larvae biomass and methionine accumulation using a kinetic model for batch cultivation and improving system performance using semi-batch cultivation. Bioprocess and Biosystems Engineering 45:333-344. DOI: 10.1007/s00449-021-02663-y.
Nguyen T, Tomberlin J, Vanlaerhoven S. 2013. Influence of resources on Hermetia illucens (Diptera: Stratiomyidae) larval development. J Med Entomol 50:898–906. DOI: 10.1603/me12260.
Noreika N, Madsen N, Jensen K, Toft S. 2016. Balancing of lipid, protein, and carbohydrate intake in a predatory beetle following hibernation, and consequences for lipid restoration. J Insect Physiol 88:1–9. DOI: 10.1016/j.jinsphys.2016.02.004.
Nyakeri EM, Ogola HJO, Ayieko MA, Amimo FA. 2017. Valorisation of organic waste material: Growth performance of wild black soldier fly larvae (Hermetia illucens) reared on different organic wastes. J Insects as Food Feed 3:193–202. DOI: 10.3920/JIFF2017.0004.
Palma L, Fernandez-Bayo J, Niemeier D, Pitesky M, VanderGheynst JS. 2019. Managing high fiber food waste for the cultivation of black soldier fly larvae. npj Sci Food 3. DOI:10.1038/s41538-019-0047-7.
Palma L, Fernández-Bayo J, Putri F, VanderGheynst JS. 2020. Almond by-product composition impacts the rearing of black soldier fly larvae and quality of the spent substrate as a soil amendment. J Sci Food Agric 100:4618–4626. DOI:10.1002/jsfa.10522.
Popa R, Green TR. 2012. Using black soldier fly larvae for processing organic leachates. J Econ Entomol 105:374–378. DOI: 10.1603/EC11192.
Puastuti W, Susana I. 2014. Potency and utilization of cocoa pod husk as an alternative feed for ruminants. Indones Bull Anim Vet Sci 24:151-159. DOI: 10.14334/wartazoa.v24i3.1072.
Rehman K ur, Rehman A, Cai M, Zheng L, Xiao X, Somroo AA, Wang H, Li W, Yu Z, Zhang J. 2017. Conversion of mixtures of dairy manure and soybean curd residue by black soldier fly larvae (Hermetia illucens L.). J Clean Prod 154:366–373. DOI:10.1016/j.jclepro.2017.04.019.
Saadoun JH, Montevecchi G, Zanasi L, Bortolini S, Macavei LI, Masino F, Maistrello L, Antonelli A. 2020. Lipid profile and growth of black soldier flies (Hermetia illucens, Stratiomyidae) reared on by-products from different food chains. J Sci Food Agric 100:3648–3657. DOI:10.1002/jsfa.10397
Schiavone A, Dabbou S, De Marco M, Cullere M, Biasato I, Biasibetti E, Capucchio MT, Bergagna S, Dezzutto D, Meneguz M, Gai F, Dalle Zotte A, Gasco L. 2018. Black soldier fly larva fat inclusion in finisher broiler chicken diet as an alternative fat source. Animal 12:2032–2039. DOI: 10.1017/S1751731117003743.
Shelomi M, Wu M, Chen S, Huang J, Burke C. 2020. Microbes associated with black soldier fly (Diptera: Stratiomiidae) degradation of food waste. Environ Entomol 49:405–411. DOI: 10.1093/ee/nvz164.
Shrestha P, Rasmussen M, Khanal SK. 2008. Solid-substrate fermentation of corn fiber by Phanerochaete chrysosporium and subsequent fermentation of hydrolysate into ethanol. J Agric Food Chem 58:3918–3924. DOI:10.1021/jf0728404.
Spranghers T, Ottoboni M, Klootwijk C, Ovyn A, Deboosere S, De Meulenaer B, Michiels J, Eeckhout M, De Clercq P, De Smet S. 2017. Nutritional composition of black soldier fly (Hermetia illucens) prepupae reared on different organic waste substrates. J Sci Food Agric 97:2594–2600. DOI: 10.1002/jsfa.8081.
Tinder AC, Puckett RT, Turner ND, Cammack JA, Tomberlin JK. 2017. Bioconversion of sorghum and cowpea by black soldier fly (Hermetia illucens (L.)) larvae for alternative protein production. J Insects as Food Feed 3:121–130. DOI:10.3920/JIFF2016.0048.
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. J Insects as Food Feed 1:249–259. DOI:10.3920/JIFF2014.0008.
Van Soest PJ, Robertson JB, Lewis BA. 1991. Methods for dietary fiber, neutral detergent fiber, and nonstarch polysaccharides in relation to animal nutrition. J Dairy Sci 74:3583–3597. DOI: 10.3168/jds.S0022-0302(91)78551-2.
Zeitz JO, Fennhoff J, Kluge H, Stangl GI, Eder K. 2015. Effects of dietary fats rich in lauric and myristic acid on performance, intestinal morphology, gut microbes, and meat quality in broilers. Poult Sci 94:2404–2413. DOI: 10.3382/ps/pev191.
Zhang J, Huang L, He J, Tomberlin JK, Li J, Lei C, Sun M, Liu Z, Yu Z. 2010. An artificial light source influences mating and oviposition of black soldier flies, Hermetia illucens. J Insect Sci 10:1536–2442. DOI: 10.1673/031.010.20201.
Zuleta-Correa A, Merino-Restrepo A, Jimenez-Correa S, Hormaza-Anaguano A, Cardona-Gallo SA. 2016. Use of white rot fungi in the degradation of an azo dye from the textile industry. DYNA 83:128-135. DOI:10.15446/DYNA.V83N198.52923.

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