PHYSICOCHEMICAL PROPERTIES OF TENEBRIO MOLITOR LARVAE FEEDING ON APPLE PEEL AND THE EFFECT OF LARVAL FERMENTATION ON THE PHENOLIC PROFILE OF APPLE PEEL

Abstract

This study explores the potential of Tenebrio molitor larvae to valorize apple peels and assesses larval fermentation’s impact on phenolics, growth potential and physicochemical properties of the larvae. Corn flour and apple peel were mixed in different ratios (1:1, 1:2, 1:4), and fermentation was conducted for 12 days. Significant changes occurred in the 1:1 ratio (EMB); larval weight increased by 62.2% compared to 58.6% in the control. After 12 days, the larvae showed increased ash, protein and carbohydrate contents, but reduced fat content. The phenolic content and antioxidant activities of the EMB medium significantly increased compared to the initial values, reaching their maximum level on day 8. Four quercetin derivatives were detected: quercetin-3-rutinoside, quercetin-3-O-glucoside, quercetin-3-O-galactoside and quercitrin. After 8 days, the amounts of quercitrin and quercetin-3-O-glucoside increased significantly. These findings suggest that T. molitor larvae can convert food waste into valuable functional food ingredients through phenolic release or conversion.

Keywords

• Tenebrio molitor
• apple peel
• phenolic compounds
• larval rearing

ELMA KABUĞUYLA BESLENEN TENEBRIO MOLITOR LARVALARININ FİZİKOKİMYASAL ÖZELLİKLERİ VE LARVAL FERMANTASYONUN ELMA KABUĞUNUN FENOLİK PROFİLİNE ETKİSİ

Abstract

Bu çalışma, Tenebrio molitor larvalarının elma kabuklarını değerlendirme potansiyeli ve larval fermantasyonun elma kabuğunda bulunan fenolik maddeler, larvaların gelişme potansiyelleri ve fizikokimyasal özellikleri üzerindeki etkilerini araştırmayı amaçlamıştır. Mısır unu ve elma kabuğu farklı oranlarda (1:1, 1:2, 1:4) karıştırılmış ve fermantasyon 12 gün boyunca gerçekleştirilmiştir. 1:1 oranındaki besiyerinde (EMB) önemli değişiklikler gözlenmiş ve larva ağırlığı, kontrol (%58.6) ile karşılaştırıldığında %62.2 oranında artış göstermiştir. 12. gün sonunda larvaların kül, protein ve karbohidrat içeriklerinde artış, ancak yağ içeriğinde azalma görülmüştür. EMB besiyerinin fenolik içeriği ve antioksidan aktiviteleri başlangıç değerlerine kıyasla önemli ölçüde artarak 8. günde maksimum seviyesine ulaşmıştır. EMB besiyerinde dört farklı kuersetin türevi tespit edilmiştir: Kuersetin-3-rutinozit, kuersetin-3-O-glukozit, kuersetin-3-O-galaktozit ve kuersitrin. 8 gün sonra, kuersitrin ve kuersetin-3-O-glukozit miktarları başlangıç değerlerine kıyasla önemli ölçüde artmıştır. Bu bulgular, T. molitor larvalarının gıda atıklarını fenolik salınım veya dönüşüm yoluyla değerli fonksiyonel gıda bileşenlerine dönüştürebileceğini göstermektedir.

Keywords

• Tenebrio molitor
• elma kabuğu
• fenolik madde
• larval fermantasyon

References

1. Andreadis, S. S., Panteli, N., Mastoraki, M., Rizou, E., Stefanou, V., Tzentilasvili, S., Sarrou, E., Chatzifotis, S., Krigas, N., Antonopoulou, E. (2022). Towards functional insect feeds: Agri-food by-products enriched with post-distillation residues of medicinal aromatic plants in Tenebrio molitor (Coleoptera: Tenebrionidae) breeding. Antioxidants, 11(1). doi: 10.3390/antiox11010068
2. Antonopoulou, E., Panteli, N., Feidantsis, K., Mastoraki, M., Koutsogeorgiou, E. I., Grivaki, E., Papagrigoriou, T., Christias, S. P., Chatzifotis, S., Lazari, D., Andreadis, S. S., Krigas, N. (2022). Carob (Ceratonia siliqua) as functional feed is beneficial in yellow mealworm (Tenebrio molitor) rearing: evidence from growth, antioxidant status and cellular responses. Antioxidants, 11(9). doi: 10.3390/antiox11091840
3. AOAC. (2000). Official methods of analysis of the association of analytical chemists. Arlington, Virginia, USA.
4. Apak, R., Güçlü, K., Özyürek, M., Karademir, S. E. (2004). Novel total antioxidant capacity index for dietary polyphenols and vitamins c and e, using their cupric ion reducing capability in the presence of neocuproine: CUPRAC method. Journal of Agricultural and Food Chemistry, 52(26), 7970–7981. doi: https://doi.org/10.1021/ jf048741x
5. Capanoglu E, Beekwilder J, Boyacioglu D, Hall R, de Vos R. (2008). Changes in antioxidant and metabolite profiles during production of tomato paste. Journal of Agricultural and Food Chemistry, 56, 964–973.
6. Catalkaya, G., Guldiken, B., Capanoglu, E. (2022). Encapsulation of anthocyanin-rich extract from black chokeberry (Aronia melanocarpa) pomace by spray drying using different coating materials. Food & Function, 13(22), 11579–11591. https://pubs.rsc.org/en/content/articlehtml/2022/fo/d2fo02569h
7. Dewanto, V., Wu, X., Adom, K. K., Liu, R. H. (2002). Thermal processing enhances the nutritional value of tomatoes by increasing total antioxidant activity. Journal of Agricultural and Food Chemistry, 50(10), 3010–3014. doi: https://doi.org/10.1021/jf0115589
8. Dhillon, G. S., Kaur, S., Brar, S. K., Verma, M. (2012). Potential of apple pomace as a solid substrate for fungal cellulase and hemicellulase bioproduction through solid-state fermentation. Industrial Crops and Products. 38, 6–13. doi: 10.1016/j.indcrop.2011.12.036

9. FAOSTAT. (2024). Crops and Livestock Products. Retrieved from https://www.fao.org/faostat/ en/#data/QCL (Erişim tarihi: 16 Temmuz 2024).
10. Gullón, B., Yáñez, R., Alonso, J. L., Parajó, J. C. (2008). L-Lactic acid production from apple pomace by sequential hydrolysis and fermentation. Bioresource Technology. 99(2), 308-319. doi: 10.1016/j.biortech.2006.12.018
11. Gulsunoglu, Z., Aravind, S., Bai, Y., Wang, L., Kutcher, H. R., Tanaka, T. (2019). Deoxynivalenol (DON) accumulation and nutrient recovery in black soldier fly larvae (Hermetia illucens) fed wheat infected with fusarium spp. Fermentation, 5(3). doi: 10.3390/ fermentation5030083
12. Gulsunoglu, Z., Purves, R., Karbancioglu-Guler, F., Kilic-Akyilmaz, M. (2020). Enhancement of phenolic antioxidants in industrial apple waste by fermentation with Aspergillus spp. Biocatalysis and Agricultural Biotechnology, 25. doi: 10.1016/j.bcab.2020.101562
13. Gulsunoglu, Zehra, Karbancioglu-Guler, F., Raes, K., Kilic-Akyilmaz, M. (2019). Soluble and insoluble-bound phenolics and antioxidant activity of various industrial plant wastes. International Journal of Food Properties, 22(1), 1501–1510. doi: 10.1080/10942912.2019.1656233
14. Gulsunoglu-Konuskan, Z., Dag, S. (2024). Physicochemical properties and ellagic acid accumulation in Tenebrio molitor larvae fed with pomegranate peel-enriched media. European Food Research and Technology, 250(5), 1473–1483. doi: 10.1007/s00217-024-04480-5
15. Gulsunoglu-Konuskan, Z., Kilic-Akyilmaz, M. (2022). Microbial bioconversion of phenolic compounds in agro-industrial wastes: a review of mechanisms and effective factors. Journal of Agricultural and Food Chemistry, 70(23), 6901–6910. doi: 10.1021/acs.jafc.1c06888
16. Harsányi, E., Juhász, C., Kovács, E., Huzsvai, L., Pintér, R., Fekete, G., Varga, Z. I., Aleksza, L., Gyuricza, C. (2020). Evaluation of organic wastes as substrates for rearing Zophobas morio, Tenebrio molitor, and Acheta domesticus larvae as alternative feed supplements. Insects. 11(9), 604. doi: 10.3390/insects11090604
17. Hernández-Carranza, P., Ávila-Sosa, R., Guerrero-Beltrán, J. A., Navarro-Cruz, A. R., Corona-Jiménez, E., Ochoa-Velasco, C. E. (2016). Optimization of antioxidant compounds extraction from fruit by-products: apple pomace, orange and banana peel. Journal of Food Processing and Preservation. 40(1), 103-115. doi: 10.1111/jfpp.12588
18. 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. doi: 10.1021/acs.jafc.7b00471
19. Jantzen da Silva Lucas, A., Menegon de Oliveira, L., da Rocha, M., Prentice, C. (2020). Edible insects: An alternative of nutritional, functional and bioactive compounds. Food Chemistry, 311(December 2019), 126022. doi: 10.1016/ j.foodchem.2019.126022
20. Kröncke, N., Benning, R. (2023). Influence of dietary protein content on the nutritional composition of mealworm larvae (Tenebrio molitor L.). Insects, 14(3), 1–19. doi: 10.3390/ insects14030261
21. Lawal, K. G., Kavle, R. R., Akanbi, T. O., Mirosa, M., Agyei, D. (2021). Enrichment in specific fatty acids profile of Tenebrio molitor and Hermetia illucens larvae through feeding. Future Foods, 3(October 2020). doi: 10.1016/j.fufo.2021.100016
22. Lees, G. L., Suttill, N. H., Wall, K. M., & Beveridge, T. H. (1995). Localization of condensed tannins in apple fruit peel, pulp, and seeds. Canadian Journal of Botany, 73(12), 1897-1904. Doi: https://doi.org/10.1139/b95-202
23. Li, L, Zhao, Z., Liu, H. (2013). Feasibility of feeding yellow mealworm (Tenebrio molitor L.) in bioregenerative life support systems as a source of animal protein for humans. Acta Astronautica, 92(1), 103–109. doi: 10.1016/ j.actaastro.2012.03.012
24. Liu, C., Masri, J., Perez, V., Maya, C., Foods, J. Z. (2020). Growth performance and nutrient composition of mealworms (Tenebrio molitor) fed on fresh plant materials-supplemented diets. Foods, 9(151), 1–10. doi: 10.3390/foods9020151
25. Madrera, R. R., Bedriñana, R. P., Valles, B. S. (2015). Production and characterization of aroma compounds from apple pomace by solid-state fermentation with selected yeasts. LWT-Food Science and Technology. doi: 10.1016/j.lwt.2015.07.056
26. Mancini, S., Fratini, F., Turchi, B., Mattioli, S., Dal Bosco, A., Tuccinardi, T., Nozic, S., Paci, G. (2019). Former foodstuff products in Tenebrio molitor rearing: Effects on growth, chemical composition, microbiological load, and antioxidant status. Animals, 9(8), 1–13. doi: 10.3390/ani9080484
27. Marks, S. C., Mullen, W., Crozier, A. (2007). Flavonoid and chlorogenic acid profiles of English cider apples. Journal of the Science of Food and Agriculture. doi: 10.1002/jsfa.2778
28. Mutha, R. E., Tatiya, A. U., Surana, S. J. (2021). Flavonoids as natural phenolic compounds and their role in therapeutics: an overview. Future Journal of Pharmaceutical Sciences. 7, 25. doi: 10.1186/s43094-020-00161-8
29. Navarro del Hierro, J., Gutiérrez-Docio, A., Otero, P., Reglero, G., Martin, D. (2020). Characterization, antioxidant activity, and inhibitory effect on pancreatic lipase of extracts from the edible insects Acheta domesticus and Tenebrio molitor. Food Chemistry, 309. doi: 10.1016/J.FOODCHEM.2019.125742
30. Oonincx, D. G. A. B., Van Broekhoven, S., Van Huis, A., Van Loon, J. J. A. (2015). Feed conversion, survival and development, and composition of four insect species on diets composed of food by-products. PLOS ONE, 10(12), e0144601. doi: 10.1371/JOURNAL.PONE.0144601
31. Rai, S., Wahile, A., Mukherjee, K., Saha, B. P., Mukherjee, P. K. (2006). Antioxidant activity of Nelumbo nucifera (sacred lotus) seeds. Journal of Ethnopharmacology, 104(3), 322–327. doi: 10.1016/J.JEP.2005.09.025
32. Rovai, D., Ortgies, M., Amin, S., Kuwahara, S., Schwartz, G., Lesniauskas, R., Garza, J., Lammert, A. (2021). Utilization of carrot pomace to grow mealworm larvae (Tenebrio molitor). Sustainability (Switzerland), 13(16). doi: 10.3390/su13169341
33. Ruschioni, S., Loreto, N., Foligni, R., Mannozzi, C., Raffaelli, N., Zamporlini, F., Pasquini, M., Roncolini, A., Cardinali, F., Osimani, A., Aquilanti, L., Isidoro, N., Riolo, P., Mozzon, M. (2020). Addition of olive pomace to feeding substrate affects growth performance and nutritional value of mealworm (Tenebrio molitor L.) larvae. Foods, 9(3). doi: 10.3390/foods9030317
34. Singleton, V. L., Orthofer, R., Lamuela-Raventós, R. M. (1999). Analysis of total phenols and other oxidation substrates and antioxidants by means of folin-ciocalteu reagent. Methods in Enzymology, 299, 152–178. doi: 10.1016/S0076-6879(99)99017-1
35. Tan, S. W., Lai, K. S., Loh, J. Y. (2018). Effects of food wastes on yellow mealworm Tenebrio molitor larval nutritional profiles and growth performances. Examines in Marine Biology & Oceanography, 2(1), 173–178. doi: 10.31031/eimbo.2018.02.000530
36. Tang, Y., Debnath, T., Choi, E. J., Kim, Y. W., Ryu, J. P., Jang, S., Chung, S. U., Choi, Y. J., Kim, E. K. (2018). Changes in the amino acid profiles and free radical scavenging activities of Tenebrio molitor larvae following enzymatic hydrolysis. PLoS ONE, 13(5), 1–14. doi: 10.1371/journal.pone.0196218
37. Van Huis, A. (2013). Potential of insects as food and feed in assuring food security. Annual Review of Entomology, 58, 563–583. https://doi.org./10.1146/annurev-ento-120811-153704.
38. Willis, J. D., Oppert, C., Jurat-Fuentes, J. L. (2010). Methods for discovery and characterization of cellulolytic enzymes from insects. Insect Science, 17(3), 184–198. doi: 10.1111/j.1744-7917.2010.01322.x
39. Xia, W., Song, B., Li, T., Liu, R. H. (2024). Phytochemical profiles, antioxidant activities, and synergistic antiproliferative effects of blueberry and apple peel extracts. Journal of the Science of Food and Agriculture. 104(2), 737–745. doi: 10.1002/jsfa.12964
40. Zhang, X., Tang, H., Chen, G., Qiao, L., Li, J., Liu, B., Liu, Z., Li, M., Liu, X. (2019). Growth performance and nutritional profile of mealworms reared on corn stover, soybean meal, and distillers’ grains. European Food Research and Technology. 245, 2631–2640. doi: 10.1007/s00217-019-03336-7