Black Soldier Fly Larvae Feed with Fermented Bamboo Culms Enriched with Lactic Acid Bacteria

Nurul Azila Abdul Razak ¹, Ang Chung Huap ^1*, Vivien Jong Yi Mian ¹, Siti Nor Ain Seri Masran ²

The study of plant-based protein source as  the nutrition of Black soldier fly

Abstract

Black soldier fly (BSF) larvae have been a promising protein source use in fish and poultry meal effectively replacing plant-based protein source. Currently, there is no study on the effects of fermented bamboo culms by lactic acid bacteria to improve the nutrition of BSF larvae. The main objective of this study is to determine the protein:fat ratio and growth rate of BSF larvae fed with fermented bamboo culm fibres (Bambusa beecheyana) enriched with lactic acid bacteria. Lactobacillus plantarum and Brevibacillus parabrevis were successfully isolated from BSF larvae gut aged 16 days and fermentation of bamboo culms fibre were successfully carried out for 21 days. Our results showed the plot VEG217 consist of Lactobacillus plantarum and Brevibacillus parabrevis (1:1) mixed with fermented bamboo culms fibre and vegetable waste have greater average weight (111%) and length (30%) compared to negative control that only consist of BSF larvae fed with vegetable waste. Interestingly, BSF larvae fed with fermented bamboo enriched with lactic acid bacteria also pupariated in much shorter time (less than 13 days) compared to negative control (18 days). All the larvae fed with fermented bamboo and lactic acid bacteria also showed improvement in the protein and fat ratio when compared to negative control (5:3).  The plot VEG111 consist of Brevibacillus parabrevis mixed with fermented bamboo and vegetable wastes have the best protein:fat ratio (4:1). This result shows the potentioal of using fermented bamboo culm fibres enriched with lactic acid bacteria to improve the growth rate of BSF larvae.

Keywords: Black Soldier Fly larvae; fermented bamboo culm fibre; lactic acid bacteria

References

Anghinoni, G., Anghinoni, F. B. G., Tormena, C. A., Braccini, A. L., de Carvalho Mendes, I., Zancanaro, L., & Lal, R. (2021). Conservation agriculture strengthen sustainability of Brazilian grain production and food security. Land Use Policy, 108, 105591. https://doi.org/10.1016/j.landusepol.2021.105591

Arasu, M. V., Al-Dhabi, N. A., Ilavenil, S., Choi, K. C., & Srigopalram, S. (2016). In vitro importance of probiotic Lactobacillus plantarum related to medical field. Saudi Journal of Biological Sciences, 23(1), S6–S10. https://doi.org/10.1016/J.SJBS.2015.09.022

Beale, D. J., Shah, R. M., Marcora, A., Hulthen, A., Karpe, A. v., Pham, K., Wijffels, G., & Paull, C. (2022). Is there any biological insight (or respite) for insects exposed to plastics? Measuring the impact on an insects central carbon metabolism when exposed to a plastic feed substrate. Science of The Total Environment, 831, 154840. https://doi.org/10.1016/j.scitotenv.2022.154840

Callegari, M., Jucker, C., Fusi, M., Leonardi, M. G., Daffonchio, D., Borin, S., Savoldelli, S., & Crotti, E. (2020). Hydrolytic Profile of the Culturable Gut Bacterial Community Associated With Hermetia illucens. Frontiers in Microbiology, 11. https://doi.org/10.3389/fmicb.2020.01965

Chen, L., Chang, J., Wang, Y., Guo, A., Liu, Y., Wang, Q., Zhu, Y., Zhang, Y., & Xie, Z. (2021). Disclosing the future food security risk of China based on crop production and water scarcity under diverse socioeconomic and climate scenarios. Science of The Total Environment, 790, 148110. https://doi.org/10.1016/j.scitotenv.2021.148110

Ding, Y., & Sherman, D. H. (2010). The Role of Synthesis and Biosynthetic Logic. In Comprehensive Natural Products II (pp. 559–579). Elsevier. https://doi.org/10.1016/B978-008045382-8.00052-6

Elbushra, A. A., & Ahmed, A. E. (2020). Food Security in Sudan: A Historical Analysis of Food Availability. Iraqi Journal of Agricultural Sciences, 51(1), 422–431.

Erkosar, B., Storelli, G., Mitchell, M., Bozonnet, L., Bozonnet, N., & Leulier, F. (2015). Pathogen Virulence Impedes Mutualist-Mediated Enhancement of Host Juvenile Growth via Inhibition of Protein Digestion. Cell Host & Microbe, 18(4), 445–455. https://doi.org/10.1016/j.chom.2015.09.001

Gayatri, G., Madhuri, P., & Bandodkar, K. B. N. (2013). Occurrence of Black Soldier Fly Hermetia illucens (Diptera: Stratiomyidae) in Biocompost. In Research Journal of Recent Sciences (Vol. 2, Issue 4). http://www.cals.ncsu.edu/waste_mgt/

Henick-Kling, Th. (1988). Yeast and Bacterial Control in Winemaking (pp. 276–316). https://doi.org/10.1007/978-3-642-83340-3_10

Hooda, R., Bhardwaj, N. K., & Singh, P. (2018). Brevibacillus parabrevis MTCC 12105: a potential bacterium for pulp and paper effluent degradation. World Journal of Microbiology and Biotechnology, 34(2). https://doi.org/10.1007/s11274-018-2414-y

Intayung, D., Chundang, P., Srikachar, S., & Kovitvadhi, A. (2021). Ontogenic development of the digestive enzymes and chemical composition of Hermetia illucens larvae of different ages. Entomologia Experimentalis et Applicata, 169(7), 665–673. https://doi.org/10.1111/eea.13063

Jambo, Y., Alemu, A., & Tasew, W. (2021). Impact of small-scale irrigation on household food security: evidence from Ethiopia. Agriculture and Food Security, 10(1). https://doi.org/10.1186/s40066-021-00294-w

Janssen, R. H., Vincken, J. P., van den Broek, L. A. M., Fogliano, V., & Lakemond, C. M. M. (2017). Nitrogen-to-Protein Conversion Factors for Three Edible Insects: Tenebrio molitor, Alphitobius diaperinus, and Hermetia illucens. Journal of Agricultural and Food Chemistry, 65(11), 2275–2278. https://doi.org/10.1021/acs.jafc.7b00471

Jenderedjian, A., & Bellows, A. C. (2021). Rural poverty, violence, and power: Rejecting and endorsing gender mainstreaming by food security NGOs in Armenia and Georgia. World Development, 140, 105270. https://doi.org/10.1016/j.worlddev.2020.105270

Khanna, S. K. (2020). Food Availability, Food Security, and Maternal Mental Health. Ecology of Food and Nutrition, 59(1), 1–2. https://doi.org/10.1080/03670244.2019.1710337

Kim, J. K., Dao, V. T., Kong, I. S., & Lee, H. H. (2010). Identification and characterization of microorganisms from earthworm viscera for the conversion of fish wastes into liquid fertilizer. Bioresource Technology, 101(14), 5131–5136. https://doi.org/10.1016/J.BIORTECH.2010.02.001

Kim, W., Bae, S., Park, K., Lee, S., Choi, Y., Han, S., & Koh, Y. (2011a). Biochemical characterization of digestive enzymes in the black soldier fly, Hermetia illucens (Diptera: Stratiomyidae). Journal of Asia-Pacific Entomology, 14(1), 11–14. https://doi.org/10.1016/j.aspen.2010.11.003

Kooienga, E. M., Baugher, C., Currin, M., Tomberlin, J. K., & Jordan, H. R. (2020). Effects of Bacterial Supplementation on Black Soldier Fly Growth and Development at Benchtop and Industrial Scale. Frontiers in Microbiology, 11. https://doi.org/10.3389/fmicb.2020.587979

Krieger-Weber, S., Heras, J. M., & Suarez, C. (2020). Lactobacillus plantarum, a new biological tool to control malolactic fermentation: A review and an outlook. In Beverages (Vol. 6, Issue 2, pp. 1–23). MDPI AG. https://doi.org/10.3390/beverages6020023

Li, X., Zhou, S., Zhang, J., Zhou, Z., & Xiong, Q. (2021). Directional changes in the intestinal bacterial community in black soldier fly (Hermetia illucens) larvae. Animals, 11(12). https://doi.org/10.3390/ani11123475

Liu, A., Ma, Y., Gunawardena, J. M. A., Egodawatta, P., & Ayoko, G. A. (2018). Ecotoxicology and Environmental Safety Heavy metals transport pathways?: The importance of atmospheric pollution contributing to stormwater pollution. Ecotoxicology and Environmental Safety, 164(August), 696–703. https://doi.org/10.1016/j.ecoenv.2018.08.072

Lorenzo, J. M., Munekata, P. E., Dominguez, R., Pateiro, M., Saraiva, J. A., & Franco, D. (2018). Main groups of microorganisms of relevance for food safety and stability: General aspects and overall description. In Innovative technologies for food preservation: Inactivation of spoilage and pathogenic microorganisms (pp. 53–107). Elsevier. https://doi.org/10.1016/B978-0-12-811031-7.00003-0

Ma, J., Lei, Y., Rehman, K. U., Yu, Z., Zhang, J., Li, W., Li, Q., Tomberlin, J. K., & Zheng, L. (2018). Dynamic Effects of Initial pH of Substrate on Biological Growth and Metamorphosis of Black Soldier Fly (Diptera: Stratiomyidae). Environmental Entomology, 47(1), 159–165. https://doi.org/10.1093/ee/nvx186

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. https://doi.org/10.1016/j.anifeedsci.2014.07.008

Martínez-Sánchez, A., Magaña, C., Saloña, M., & Rojo, S. (2011). First record of Hermetia illucens (Diptera: Stratiomyidae) on human corpses in Iberian Peninsula. Forensic Science International, 206(1–3). https://doi.org/10.1016/j.forsciint.2010.10.021

Matejceková, Z., Liptáková, D., Spodniaková, S., & Valík, L. (2016). Characterization of the growth of Lactobacillus plantarum in milk in dependence on temperature . Acta Chimica Slovaca, 9(2), 104–108. https://doi.org/10.1515/acs-2016-0018

Mazza, L., Xiao, X., ur Rehman, K., Cai, M., Zhang, D., Fasulo, S., Tomberlin, J. K., Zheng, L., Soomro, A. A., Yu, Z., & Zhang, J. (2020). Management of chicken manure using black soldier fly (Diptera: Stratiomyidae) larvae assisted by companion bacteria. Waste Management, 102, 312–318. https://doi.org/10.1016/j.wasman.2019.10.055

Meneguz, M., Gasco, L., & Tomberlin, J. K. (2018). Impact of pH and feeding system on black soldier fly (Hermetia illucens, L; Diptera: Stratiomyidae) larval development. PLoS ONE, 13(8). https://doi.org/10.1371/journal.pone.0202591

Moula, N., & Detilleux, J. (2019). A meta-analysis of the effects of insects in feed on poultry growth performances. Animals, 9(5). https://doi.org/10.3390/ani9050201

Nielsen, A. L., & Hamilton, G. C. (2009). Seasonal occurrence and impact of halyomorpha halys (Hemiptera: Pentatomidae) in tree fruit. Journal of Economic Entomology, 102(3), 1133–1140. https://doi.org/10.1603/029.102.0335

Parichehreh, S., Tahmasbi, G., Sarafrazi, A., Imani, S., & Tajabadi, N. (2018). Isolation and identification of Lactobacillus bacteria found in the gastrointestinal tract of the dwarf honey bee, Apis florea Fabricius, 1973 (Hymenoptera: Apidae). Apidologie, 49(3), 430–438. https://doi.org/10.1007/s13592-018-0569-z

Raio, A., Roversi, P. F., & Francardi, V. (2016). Bacteria associated to Rhynchophorus ferrugineus (Olivier) (Coleoptera dryophthoridae) in Italy. Redia, 99, 53–57. https://doi.org/10.19263/REDIA-99.16.11

Ravi, H. K., Degrou, A., Costil, J., Trespeuch, C., Chemat, F., & Vian, M. A. (2020). Larvae mediated valorization of industrial, agriculture and food wastes: Biorefinery concept through bioconversion, processes, procedures, and products. In Processes (Vol. 8, Issue 7). MDPI AG. https://doi.org/10.3390/PR8070857

Renna, M., Schiavone, A., Gai, F., Dabbou, S., Lussiana, C., Malfatto, V., Prearo, M., Capucchio, M. T., Biasato, I., Biasibetti, E., de Marco, M., Brugiapaglia, A., Zoccarato, I., & Gasco, L. (2017). Evaluation of the suitability of a partially defatted black soldier fly (Hermetia illucens L.) larvae meal as ingredient for rainbow trout (Oncorhynchus mykiss Walbaum) diets. Journal of Animal Science and Biotechnology, 8(1). https://doi.org/10.1186/s40104-017-0191-3

Salami, S. A., Ewulo, B., & Adewole, W. A. (2021). Farmer’s Perception on the Benefits of Poultry Production in Abuja Municipal Area Council, Federal Capital Territory, Nigeria. Nigerian Agricultural Journal, 52(1), 96–101. http://www.ajol.info/index.php/najhttps://www.naj.asn.org

Schiavone, A., de Marco, M., Martínez, 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(1). https://doi.org/10.1186/s40104-017-0181-5

Schwarzer, M., Makki, K., Storelli, G., Machuca-Gayet, I., Srutkova, D., Hermanova, P., Martino, M. E., Balmand, S., Hudcovic, T., Heddi, A., Rieusset, J., Kozakova, H., Vidal, H., & Leulier, F. (2016). Lactobacillus plantarum strain maintains growth of infant mice during chronic undernutrition. Science, 351(6275), 854–857. https://doi.org/10.1126/science.aad8588

Somroo, A. A., ur Rehman, K., Zheng, L., Cai, M., Xiao, X., Hu, S., Mathys, A., Gold, M., Yu, Z., & Zhang, J. (2019). Influence of Lactobacillus buchneri on soybean curd residue co-conversion by black soldier fly larvae (Hermetia illucens) for food and feedstock production. Waste Management, 86, 114–122. https://doi.org/10.1016/j.wasman.2019.01.022

Spranghers, T., Michiels, J., Vrancx, J., Ovyn, A., Eeckhout, M., de Clercq, P., & de Smet, S. (2018). Gut antimicrobial effects and nutritional value of black soldier fly ( Hermetia illucens L.) prepupae for weaned piglets. Animal Feed Science and Technology, 235, 33–42. https://doi.org/10.1016/j.anifeedsci.2017.08.012

Storelli, G., Defaye, A., Erkosar, B., Hols, P., Royet, J., & Leulier, F. (2011). Lactobacillus plantarum promotes drosophila systemic growth by modulating hormonal signals through TOR-dependent nutrient sensing. Cell Metabolism, 14(3), 403–414. https://doi.org/10.1016/j.cmet.2011.07.012

Sumbule, E. K., Ambula, M. K., Osuga, I. M., Changeh, J. G., Mwangi, D. M., Subramanian, S., Salifu, D., Alaru, P. A. O., Githinji, M., van Loon, J. J. A., Dicke, M., & Tanga, C. M. (2021). Cost-effectiveness of black soldier fly larvae meal as substitute of fishmeal in diets for layer chicks and growers. Sustainability (Switzerland), 13(11). https://doi.org/10.3390/su13116074

Talib, A., Onn, K. K., Chowdury, M. A., Din, W. M. W., & Yahya, K. (2017). The beneficial effects of multispecies Bacillus as probiotics in enhancing culture performance for mud crab Scylla paramamosain larval culture. Aquaculture International, 25(2), 849–866. https://doi.org/10.1007/s10499-016-0070-5

Valan Arasu, M., Jung, M.-W., Ilavenil, S., Jane, M., Kim, D.-H., Lee, K.-D., Park, H.-S., Hur, T.-Y., Choi, G.-J., Lim, Y.-C., Al-Dhabi, N. A., & Choi, K.-C. (2013). Isolation and characterization of antifungal compound from Lactobacillus plantarum KCC-10 from forage silage with potential beneficial properties. Journal of Applied Microbiology, 115(5), 1172–1185. https://doi.org/10.1111/jam.12319

Walton, G. E., Gibson, G. R., & Hunter, K. A. (2021). Mechanisms linking the human gut microbiome to prophylactic and treatment strategies for COVID-19. British Journal of Nutrition, 126(2), 219–227. https://doi.org/10.1017/S0007114520003980

Wang, Z., Li, P., Luo, L., Simpson, D. J., & Gänzle, M. G. (2018). Daqu Fermentation Selects for Heat-Resistant Enterobacteriaceae and Bacilli. Applied and Environmental Microbiology, 84(21). https://doi.org/10.1128/AEM.01483-18

Wissinger, S., Eldermire, C., & Whissel, J. (2004). The role of larval cases in reducing aggression and cannibalism among caddisflies in temporary wetlands. Wetlands, 24(4), 777–783.

Won, T. J., Kim, B., Lee, Y., Bang, J. S., Oh, E. S., Yoo, J. S., Hyung, K. E., Yoon, J., Hwang, S., Park, E. S., Park, S. Y., & Hwang, K. W. (2012). Therapeutic potential of Lactobacillus plantarum CJLP133 for house-dust mite-induced dermatitis in NC/Nga mice. Cellular Immunology, 277(1–2), 49–57. https://doi.org/10.1016/J.CELLIMM.2012.05.013

 Zhang, Y.-S., Li, X.-P., Liu, H.-M., Yao-Kun, Z., Zhao, F.-F., Qin-Jie, Y. U., Li, H., & Jian-Wen, C. (2013). Study on universal cleaning solution in removing blended pesticide residues in Chinese cabbage. 5(8), 202–207. https://doi.org/10.5897/JECE