اثرات جایگزینی پودر لارو سوسک زرد (Tenebrio molitor) به جای پودر ماهی بر عملکرد رشد، برخی پارامترهای خون و کبد فیل ماهی (Huso huso)

نوع مقاله : مقاله پژوهشی

نویسندگان

گروه شیلات، دانشکده علوم دامی و شیلات، دانشگاه علوم کشاورزی و منابع طبیعی ساری، ساری، مازندران

چکیده

با توجه به محدودیت تولید پودر ماهی، استفاده از جایگزین­ های تأمین­ کننده پروتئین از جمله پودر حشرات اهمیت بالایی در آبزی‌پروری پایدار دارد. این مطالعه با هدف بررسی اثرات جایگزینی سطوح مختلف پودر لارو سوسک زرد (میلورم) (Tenebrio molitor) به جای پودر ماهی بر رشد، فرآسنجه­ های خونی، شاخص‌های بیوشیمیایی سرم و آنزیم‌های کبدی فیل ماهی (Huso huso) انجام شد. تعداد 360 فیل ماهی (9 ± 8/112 گرم) به طور کاملاً تصادفی در 6 تیمار (هر کدام با سه تکرار) توزیع و با جیره‌های حاوی سطوح صفر (شاهد)، 20، 40، 60، 80 و 100% پودر میلورم به جای پودر ماهی به مدت 8 هفته تغذیه شدند. نتایج نشان داد که بالاترین افزایش وزن بدن و نرخ رشد ویژه در تیمارهای 40 و 60% پودر لارو سوسک زرد حاصل می‌شود (05/0>P). بازماندگی ماهیان تفاوت معنی­داری بین تیمارها نشان نداد (05/0P>). کمترین میزان ضریب تبدیل غذایی در ماهیان تغذیه ­شده بین سطوح جایگزینی 20 تا 60% پودر میلورم و بالاترین مقدار آن در ماهیان گروه شاهد دیده شد (05/0>P). شاخص­های خونی شامل تعداد گلبول سفید، گلبول قرمز، هموگلوبین و هماتوکریت با افزایش سطح جایگزینی پودر میلورم کاهش یافته و کمترین میزان در جایگزینی کامل با پودر میلورم حاصل شد (05/0>P). بجز گروه 100%، میزان آلبومین و پروتئین تام در دیگر گروه‌ها در مقایسه با گروه شاهد بهبود یافت (05/0P<). کمترین میزان گلوکز و کلسترول خون در گروه شاهد مشاهده شد. غلظت تری‌گلیسرید در گروه 20% پودر میلورم اختلاف معنی­داری با گروه شاهد نداشت (05/0P>)، ولی در سطوح بالاتر از آن به‌شدت کاهش یافت (05/0P<). مقادیر آنزیم‌های کبدی AST، ALT و ALP با گنجاندن پودر میلورم کاهش یافت (05/0P<). بر اساس نتایج، امکان جایگزینی کامل پودر میلورم به­جای پودر ماهی در جیره فیل‌ماهی وجود نداشته و سطح جایگزینی 20% به عنوان سطح بهینه پیشنهاد می‌شود.

کلیدواژه‌ها

موضوعات


عنوان مقاله [English]

Effects of dietary replacement of fish meal by yellow larval mealworm (Tenebrio molitor) on growth performance, some blood and liver parameters in Beluga (Huso huso)

نویسندگان [English]

  • Seyed Ali Asghar Bagheri Khamkhaneh
  • Abolghasem Esmaeili Fereidouni
  • Sakineh Yeganeh
  • Hossein Oraji
Department of Fisheries, Faculty of Animals Sciences and Fisheries, Sari Agricultural Sciences and Natural Resource University, Sari, Mazandaran, Iran
چکیده [English]

Introduction: Aquaculture is the fastest-growing source of animal protein globally and currently provides nearly half of the world's seafood consumption. Due to the limited fishery resources from ocean catches, this shortfall must be addressed through the aquaculture industry. To tackle the issues of fishmeal shortages in recent decades, special attention has been given to the use of alternatives such as insects in aquaculture feed. Insects are one of the most diverse animal groups in the world, with some species possessing suitable nutritional value. Among insects, the yellow mealworm Tenebrio molitor stands out due to its high protein and fat contents. It also contains considerable amounts of bioactive compounds and chitin with antioxidant potential, antibacterial peptides, and other immune stimulants that enhance immunity and improves hematological parameters in various aquatic species. In this study, the effects of replacing fishmeal with the yellow mealworm larvae meal were investigated on blood parameters, serum biochemical composition, and liver enzymes in Beluga, Huso huso.
Materials and methods: A total of 360 fish with an average weight of approximate 112.9 ± 8.0 g were randomly distributed to polyethylene circular tanks with a capacity of 1500 liters. The experimental treatments (each with three replicates) included the replacement of 0% (control), 20%, 40%, 60%, 80%, and 100% of yellow larval mealworm (MW) meal with fish meal. At the end of the trial, blood sampling was performed using a syringe from the fish's caudal fin. The counting of red blood cells and white blood cells was done using a hemocytometer (Neubauer), and the hematocrit was measured through the microhematocrit method, while the hemoglobin concentration was measured by the cyanmethemoglobin method using a spectrophotometer at a wavelength of 540 nm in grams per deciliter. Liver enzyme levels including alkaline phosphatase (ALP), aspartate aminotransferase (AST), and alanine aminotransferase (ALT) were measured using the α-ketoglutarate method. Lactate dehydrogenase (LDH) was tested using the lactate-pyruvate method to determine the possibility of tissue damage. Data analysis was performed using One-Way ANOVA and Duncan's multiple range comparison tests were performed at a significance level of P<0.05.
Results: According to the results of growth indices, the highest body weight gain and specific growth rate were achieved in treatments substituted with 40% and 60% MW (P<0.05). The survival rate of the fish did not show a significant difference between the treatments (P>0.05). The number of white blood cells, red blood cells, hemoglobin, and hematocrit decreased as mealworm powder increased in diet, with the lowest values observed in 100% MW (P>0.05). The values of MCH and MCHC significantly decreased with 100% MW replacement (P>0.05). Lymphocyte numbers were significantly higher in 40% and 60% MW groups compared to the 20% (P>0.05). The values of albumin and total protein improved with dietary replacement of MW powder, except for the 100% replacement (P<0.05). The concentration of triglycerides in group with 20% MW was similar to that of the control (P<0.05); however, it decreased as the MW replacement increased (P<0.05). Hepatic enzymes such as AST, ALT, and ALP decreased with the inclusion of MW in the diet (P<0.05).
Discussion: Total protein and albumin play an important role in immune responses, and the improvement of these parameters in the current study may indicate enhanced immunity in beluga after replacing fishmeal with MW. Additionally, diets containing insect meal improve the microbial composition of the digestive system, ultimately affecting fish immunity and health. Chitin also regulates fat metabolism by preventing the hepatic circulation of bile acids and interfering with the natural digestion and absorption of fats in the intestine and the biosynthesis of fatty acids in the liver.
Conclusion: Based on the results, it is not feasible to completely replace MW meal with fishmeal, and a 20% replacement level is suggested as the optimal for beluga. However, substitution levels up to 40-60% may also be considered with caution.

کلیدواژه‌ها [English]

  • Insects meal
  • Protein
  • Hematology
  • Liver enzymes
  • Sturgeon
Alfiko, Y., Retno, D.X., Astuti, T., Wong, J., Wang, L. 2022. Insects as a feed ingredient for fish culture: Status and trends. Aquaculture and Fisheries 7: 166-178. DOI: 10.1016/j.aaf.2021.10.004.
 
Anany, E.M., Ibrahim, M.A., El-Razek, I.M.A., El-Nabawy, E.S.M., Amer, A.A., Zaineldin, A.I., Gewaily, M.S., Dawood, M.A. 2023. Combined effects of yellow mealworm (Tenebrio molitor) and Saccharomyces cerevisiae on the growth performance, feed utilization intestinal health, and blood biomarkers of Nile tilapia (Oreochromis niloticus) fed fish meal-free diets. Probiotics and Antimicrobial Proteins 32: 1-12. DOI: 10.1007/s12602-023-10199-8.
 
Arru, B., Furesi, R., Gasco, L., Madau, F.A., Pulina, P. 2019. The introduction of insect meals into fish diet: The first economic analysis on European sea bass farming. Sustainability 11: 1697. DOI: 10.3390/su11061697.
 
Ates, B., Orun, I., Talas, Z.S., Durmaz, G., Yilmaz, I. 2008. Effects of sodium selenite on some biochemical and hematological parameters of rainbow trout (Oncorhynchus mykiss Walbaum, 1792) exposed to Pb2+ and Cu2+. Fish Physiology and Biochemistry 34: 53-59. DOI: 10.1007/s10695-007-9146-5.
 
Bahmani, M., Kazemi, R., Donskaya, P. 1999. Comparative study of biochemical and hematological features in reared sturgeons. Iranian Journal of Fisheries Science 1: 61-73. DOI: 20.1001.1.15622916.1999.1.2.6.2.
 
Barrett, M., Godfrey, R.K., Schnell, A., Fischer, B. 2024. Farmed yellow mealworm (Tenebrio molitor; Coleoptera: Tenebrionidae) welfare: species-specific recommendations for a global industry. Journal of Insects as Food and Feed 10: 903-948. DOI: 10.1163/23524588-20230104.
 
Barroso, F.G., de Haro, C., Sanchez-Muros, M.J., Venegas, E., Martínez-Sanchez, A., Perez-Banon, C. 2014. The potential of various insect species for use as food for fish. Aquaculture 422-423: 193-201. DOI: 10.1016/j.aquaculture.2013.12.024.
 
Belforti, M., Gai, F., Lussiana, C., Renna, M., Malfatto, V., Rotolo, L., De Marco, M., Dabbou, S., Schiavone, A., Zoccarato, I., Gasco, L. 2015. Tenebrio molitor meal in rainbow trout (Oncorhynchus mykiss) diets: effects on animal performance, nutrient digestibility and chemical composition of fillets. Italian Journal of Animal Science 14: 670-676. DOI: 10.4081/ijas.2015.4170.
 
Belghit, I., Liland, N.S., Gjesdal, P., Biancarosa, I., Menchetti, E., Li, Y., Waagbø, R., Krogdahl., Å., Lock, E.J. 2019. Black soldier fly larvae meal can replace fish meal in diets of sea-water phase Atlantic salmon (Salmo salar). Aquaculture 503: 609-619. DOI: 10.1016/j.aquaculture.2018.12.032.
 
Binaii, M., Ghiasi, M., Farabi, S. M. V., Pourgholam, R., Fazli, H., Safari, R., Alavi, E., Taghavi, M.J., Bankehsaz, Z. 2014. Biochemical and hemato-immunological parameters in juvenile beluga (Huso huso) following the diet supplemented with nettle (Urtica dioica). Fish and Shellfish Immunology 36: 46-51. DOI: 10.1016/j.fsi.2013.10.001.
 
Blaxhall, P., Daisley, K. 1973. Routine haematological methods for use with fish blood. Journal of Fish Biology 5: 771-781. DOI: 10.1111/j.1095-8649.1973. tb045 10.x.
 
Borges, A., Scotti, L.V., Siqueira, D.R., Jurinitz, D.F., Wassermann, G.F. 2004. Hematologic and serum biochemical values for jundiá (Rhamdia quelen). Fish Physiology and Biochemistry 30: 21-25. DOI: 10.1007/s10695-004-5000-1.
 
Brafield, A.E. 1985. Laboratories studies on energy budgets. In: Fish Energetic. New Perspective. Tytler, P., Calow, P. (Eds.). Croom Helm, London, 257-281.
 
Caimi, C., Renna, M., Lussiana, C., Bonaldo, A., Gariglio, M., Meneguz, M., Dabbou, S., Schiavone, A., Gai, F., Elia, A.C., Prearo, M., Gasco, L. 2020a. First insights on black soldier fly (Hermetia illucens L.) larvae meal dietary administration in Siberian sturgeon (Acipenser baerii Brandt) juveniles. Aquaculture 515: 734539. DOI: 10.1016/j.aquaculture.2019. 734539.
 
Caimi, C., Gasco, L., Biasato, I., Malfatto, V., Varello, K., Prearo, M., Pastorino, P., Bona, M.C., Francese, D.R., Schiavone, A., Elia, A.C., Dörr, A.J.M., Gai, F. 2020b. Could dietary black soldier fly meal inclusion affect the liver and intestinal histological traits and the oxidative stress biomarkers of Siberian sturgeon (Acipenser baerii) juveniles? Animals 10: 155. DOI: 10.3390/ani10010155.
 
Campbell, T.W., Ellis, C.K. 2007. Avian and Exotic Animal Hematology and Cytology. 3rd edn. Blackwell Publishing, Ames. 287 p.
 
Cashion, T., Le Manach, F., Zeller, D., Pauly, D. 2017. Most fish destined for fishmeal production are food-grade fish. Fish and Fisheries 18: 837-844. DOI: 10.1111/faf.12209.
 
Chen, H., Yu, J., Ran, X., Wu, J., Chen, Y., Tan, B., Lin, S. 2023. Effects of yellow mealworm (Tenebrio molitor) on growth performance, hepatic health and digestibility in juvenile Largemouth Bass (Micropterus salmoides). Animals 13: 1389. DOI: 10.3390/ani13081389.
 
Doumas, B.T., Watson, W.A., Biggs, H.G. 1971. Albumin standards and the measurement of serum albumin with bromcresol green. Clinica Chimica Acta 31: 87-96. DOI: 10.1016/0009-8981(71)90365-2.
 
Dumas, A., Raggi, T., Barkhouse, J., Lewis, E., Weltzien, E. 2018. The oil fraction and partially defatted meal of black soldier fly larvae (Hermetia illucens) affect differently growth performance, feed efficiency, nutrient deposition, blood glucose and lipid digestibility of rainbow trout (Oncorhynchus mykiss). Aquaculture 492: 24-34. DOI: 10.1016/j.aquaculture.2018.03.038.
 
Falahatkar, B., Alaf Noveirian, H., Ghafouri, H., Babakhani, A. 2017. Effect of different temperature regimes on blood parameters of Acipenser ruthenus during a simulated transport experiment. Journal of Animal Research (Iranian Journal of Biology) 30: 225-236. DOI: 20.1001.1.23832614.1396.30.2.10.1.
 
Fall, S.K.L., Fall, J., Loum, A., Sagne, M., Jatta, S., Ndong, D., Diouf, M., Sheen, S.S. 2020. Effects of partial substitution of fish meal by Crustacean (Callianassa) meal on the growth performance, feed efficiency and survival rate of Nile tilapia (Oreochromis niloticus). Journal of Biology and Life Science 11: 207-217. DOI: 10.5296/jbls.v11i1.16700.
 
Feng, P., He, J., Lv, M., Huang, G., Chen, X., Yang, Q., Wang, J., Wang, D., Ma, H. 2019. Effect of dietary Tenebrio molitor protein on growth performance and immunological parameters in Macrobrachium rosenbergii. Aquaculture 511: 734247. DOI: 10.1016/j.aquaculture.2019.734247.
 
Finke, M.D. 2002. Complete nutrient composition of commercially raised invertebrates used as food for insectivores. Zoo Biology 21: 269-285. DOI: 10.1002/zoo.10031.
 
Gasco, L., Henry, M., Piccolo, G., Marono, S., Gai, F., Renna, M., Lussiana, C., Antonopoulou, E., Mola, P., Chatzifotis, S. 2016. Tenebrio molitor meal in diets for European sea bass (Dicentrarchus labrax L.) juveniles: growth performance, whole body composition and in vivo apparent digestibility. Animal Feed Science and Technology 220: 34-45. DOI: 10.1016/j.anifeedsci.2016.07.003.
 
Gasco, L., Acuti, G., Bani, P., Dalle Zotte, A., Danieli, P.P., De Angelis, A. 2020. Insect and fish by-products as sustainable alternatives to conventional animal proteins in animal nutrition. Italian Journal of Animal Science 19: 360-372. DOI: 10.1080/1828051X.2020.1743209.
 
Gopalakannan, A., Arul, V. 2006. Immunomodulatory effects of dietary intake of chitin, chitosan and levamisole on the immune system of Cyprinus carpio and control of Aeromonas hydrophila infection in ponds. Aquaculture 255: 179-187. DOI: 10.1016/j.aquaculture.2006.01.012.
 
Gutowska, M.A., Drazen, J.C., Robison, B.H. 2004. Digestive chitinolytic activity in marine fishes of Monterey Bay, California. Comparative Biochemistry and Physiology 139A: 351-358. DOI: 10.1016/j.cbpb.2004.09.020.
 
Habte-Tsion, H.M., Hawkyard, M., Sealey, W.M., Bradshaw, D., Meesala, K.M., Bouchard, D.A. 2024. Effects of fishmeal substitution with mealworm meals (Tenebrio molitor and Alphitobius diaperinus) on the growth, physiobiochemical response, digesta microbiome, and immune genes expression of Atlantic salmon (Salmo salar). Aquaculture Nutrition 1: 1-21. DOI: 10.1155/2024/6618117.
 
Halver, J.E., Hardy, R.W. 2002. Fish Nutrition. Elsevier, Amsterdam, Netherlands, 839 p.
 
Harikrishnan, R., Kim, J.S., Balasundaram, C., Heo, M.S. 2012. Dietary supplementation with chitin and chitosan on haematology and innate immune response in Epinephelus bruneus against Philasterides dicentrarchi. Experimental Parasitology 131: 116-124. DOI: 10.1016/j.exppara.2012.03.020.
 
Harsij, M., Adineh, H., Maleknejad, R., Jafariyan, H., Asadi, M. 2019. The use of live mealworm (Tenebrio molitor) in diet of rainbow trout (Oncorhynchus mykiss): effect on growth performance and survival, nutritional efficiency, carcass compositions and intestinal digestive enzymes. Journal of Fisheries Science and Technology 8: 137-143. DOI: 20.1001.1.23225513.1398.8.3.3.3.
 
Henry, M.A., Gai, F., Enes, P., Perez-Jimenez, A., Gasco, L. 2018. Effect of partial dietary replacement of fish meal by yellow mealworm (Tenebrio molitor) larvae meal on the innate immune response and intestinal antioxidant enzymes of rainbow trout (Oncorhynchus mykiss). Fish and Shellfish Immunology 83: 308-313. DOI: 10.1016/j.fsi.2018. 09.040.
 
Hoffmann, L., Rawski, M., Nogales-Merida, S., Mazurkiewicz, J. 2020. Dietary inclusion of Tenebrio molitor meal in sea trout larvae rearing: Effects on fish growth performance, survival, condition, and GIT and liver enzymatic activity. Annals of Animal Science 20: 579-598. DOI: 10.2478/aoas-2020-0002.
 
Iaconisi, V., Bonelli, A., Pupino, R., Gai, F., Parisi, G. 2018. Mealworm as dietary protein source for rainbow trout: Body and fillet quality traits. Aquaculture 484: 197-204. DOI: 10.1016/j.aquaculture.2017.11.034.
 
Jeong, S.M., Khosravi, S., Mauliasari, I.R., Lee, S.M. 2020. Dietary inclusion of mealworm (Tenebrio molitor) meal as an alternative protein source in practical diets for rainbow trout (Oncorhynchus mykiss) fry. Fisheries and Aquatic Sciences 23: 1-8. DOI: 10.1186/s41240-020-00158-7.
 
Józefiak, A., Nogales-Mérida, S., Rawski, M., Kierończyk, B., Mazurkiewicz, J. 2019. Effects of insect diets on the gastrointestinal tract health and growth performance of Siberian sturgeon (Acipenser baerii Brandt, 1869). BMC Veterinary Research 15: 348. DOI: 10.1186/s12917-019-2070-y.
 
Khosravi, S., Kim, E., Lee, Y.S., Lee, S.M. 2018. Dietary inclusion of mealworm (Tenebrio molitor) meal as an alternative protein source in practical diets for juvenile rockfish (Sebastes schlegeli). Entomological Research 48: 214-221. DOI: 10.1111/1748-5967.12306.
 
Langston, K., Selaledi, L., Tanga, C., Yusuf, A. 2024. The nutritional profile of the yellow mealworm larvae (Tenebrio molitor) reared on four different substrates. Future Foods 9: 100388. DOI: 10.1016/j.fufo.2024.100388.
 
Li, S., Ji, H., Zhang, B., Zhou, J., Yu, H. 2017. Defatted black soldier fly (Hermetia illucens) larvae meal in diets for juvenile Jian carp (Cyprinus carpio var. Jian): Growth performance, antioxidant enzyme activities, digestive enzyme activities, intestine and hepatopancreas histological structure. Aquaculture 477: 62-70. DOI: 10.1016/j.aquaculture.2017.04.015.
 
Liland, N.S., Araujo, P., Xu, X.X., Lock, E.J., Radhakrishnan, G., Prabhu, A.J.P., Belghit, I. 2021. A meta-analysis on the nutritional value of insects in aquafeeds. Journal of Insects Food Feed 7: 743-759. DOI: 10.3920/JIFF2020.0147.
 
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. DOI: 10.1016/j.anifeedsci.2014.07.008.
 
Mastoraki, M., Mollá Ferrándiz, P., Vardali, S.C., Kontodimas, D.C., Kotzamanis, Y.P., Gasco, L., Chatzifotis, S., Antonopoulou, E. 2020. A comparative study on the effect of fish meal substitution with three different insect meals on growth, body composition and metabolism of European sea bass (Dicentrarchus labrax L.). Aquaculture 528: 735511. DOI: 10.1016/j.aquaculture.2020.735511.
 
McClatchey, K.D. 2002. Clinical Laboratory Medicine, 2nd edn. Lippincott Williams and Wilkins, Philadelphia, 1936 p.
 
Melenchón, F., Larrán, A.M., De Mercado, E., Hidalgo, M.C., Cardenete, G., Barroso, F.G., Fabrikov, D., Lourenço, H.M., Pessoa, M.F., Tomás-Almenar, C. 2021. Potential use of black soldier fly (Hermetia illucens) and mealworm (Tenebrio molitor) insect meals in diets for rainbow trout (Oncorhynchus mykiss). Aquaculture Nutrition 27: 491-505. DOI: 10.1111/anu.13201.
 
New, M.B., Wijksto, M.U.N. 2002. Use of Fish meal and Fish Oil in Aquafeeds: Further Thoughts on the Fishmeal Trap. FAO Fisheries Circular No. 975 FIPP/C975. Food and Agriculture Organization of the United Nations, Rome.
 
Ng, W., Liew, F., Ang, L., Wong, K. 2001. Potential of mealworm (Tenebrio molitor) as an alternative protein source in practical diets for African catfish, Clarias gariepinus. Aquaculture Research 32: 273-280. DOI: 10.1046/j.1355-557x.2001.00024.x.
 
Nogales-Mérida, S., Gobbi, P., Józefiak, D., Mazurkiewicz, J., Dudek, K., Rawski, M., Kierończyk, B., Józefiak, A. 2019. Insect meals in fish nutrition. Reviews in Aquaculture 11: 1080-1103. DOI: 10.1111/raq.12281.
 
Piccolo, G., Iaconisi, V., Marono, S., Gasco, L., Loponte, R., Nizza, S., Bovera, F., Parisi, G. 2017. Effect of Tenebrio molitor larvae meal on growth performance, in vivo nutrients digestibility, somatic and marketable indexes of gilthead sea bream (Sparus aurata). Animal Feed Science and Technology 226: 12-20. DOI: 10.1016/j.anifeedsci.2017.02.007.
 
Pyka, J., Kolman, R. 2003. Feeding intensity and growth of Siberian sturgeon Acipenser baerii Brandt in pond cultivation. Archives of Polish Fisheries 11: 287-294. DOI: 10.11/APS-1201-8.
 
Raghuvaran, N., Varghese, T., Jana, P., Angela Brighty, R.J., Muthiah Sethupathy, A., Sudarshan, S., Alrashdi, Y.B.A., Ibrahim, A.E., El Deeb, S. 2024. Current status and global research trend patterns of insect meal in aquaculture from scientometric perspective: (2013-2022). Aquaculture Nutrition 1: 1-20. DOI: 10.1155/2024/5466604.
 
Rawski, M., Mazurkiewicz, J., Kierończyk, B., Józefiak, D. 2020. Black soldier fly full-fat larvae meal as an alternative to fish meal and fish oil in Siberian sturgeon nutrition: The effects on physical properties of the feed, animal growth performance, and feed acceptance and utilization. Animals 10: 2119. DOI: 10.3390/ani10112119.
 
Rawski, M., Mazurkiewicz, J., Kieronczyk, B., Józefiak, D. 2021. Black soldier fly full-fat larvae meal is more profitable than fish meal and fish oil in Siberian sturgeon farming: The effects on aquaculture sustainability, economy and fish GIT development. Animals 11: 604. DOI: 10.3390/ani11030604.
 
Ribeiro, N., Abelho, M., Costa, R. 2018. A review of the scientific literature for optimal conditions for mass rearing Tenebrio molitor (Coleoptera: Tenebrionidae). Journal of Entomological Science 53: 434-454. DOI: 10.18474/JES17-67.1.
 
Sánchez-Muros, M.J., de Haro, C., Sanz, A., Trenzado, C.E., Villareces, S., Barroso, F.G. 2016. Nutritional evaluation of Tenebrio molitor meal as fishmeal substitute for tilapia (Oreochromis niloticus) diet. Aquaculture Nutrition 22: 943-955. DOI: 10.1111/anu.12313.
 
Sankian, Z., Khosravi, S., Kim, Y.O., Lee, S.M. 2018. Effects of dietary inclusion of yellow mealworm (Tenebrio molitor) meal on growth performance, feed utilization, body composition, plasma biochemical indices, selected immune parameters and antioxidant enzyme activities of mandarin fish (Siniperca scherzeri) juveniles. Aquaculture 496: 79-87. DOI: 10.1016/j.aquaculture.2018.07.012.
 
Scaffardi, L., Formici, G. 2022. Novel Foods and Edible Insects in the European Union: An Interdisciplinary Analysis. Springer, Amsterdam, 181 p.
 
Singh, S.K., Pawar, L., Thomas, A.J., Debbarma, R., Biswas, P., Ningombam, A., Devi, A.G., Waikhom, G., Patel, A.B., Meena, K.D., Chakraborty, G. 2024. The current state of research and potential applications of insects for resource recovery and aquaculture feed. Environmental Science and Pollution Research 31: 62264-62282. DOI: 10.1007/s11356-023-29068-6.
 
Su, J., Gong, Y., Cao, S., Lu, F., Han, D., Liu, H., Jin, J., Yang, Y., Zhu, X., Xie, S. 2017. Effects of dietary Tenebrio molitor meal on the growth performance, immune response and disease resistance of yellow catfish (Pelteobagrus fulvidraco). Fish and Shellfish Immunology 69: 59-66. DOI: 10.1016/j.fsi.2017.08.008.
 
Su, J., Liu, Y., Xi, L., Lu, Q., Liu, H., Jin, J., Yang, Y., Zhu, X., Han, D., Xie, S. 2022. The effect of dietary Tenebrio molitor meal inclusion on growth performance and liver health of largemouth bass (Micropterus salmoides). Journal of Insects as Food and Feed 8: 1297-1309. DOI: 10.3920/JIFF2021.0033.
 
Taufek, N.M., Aspani, F., Muin, H., Raji, A.A., Razak, S.A. Alias, Z. 2016. The effect of dietary cricket meal (Gryllus bimaculatus) on growth performance, antioxidant enzyme activities, and haematological response of African catfish (Clarias gariepinus). Fish Physiology and Biochemistry 42: 1143-1155. DOI: 10.1007/s10695-016-0204-8.
 
Terova, G., Gini, E., Gasco, L., Moroni, F., Antonini, M., Rimoldi, S. 2021. Effects of full replacement of dietary fishmeal with insect meal from Tenebrio molitor on rainbow trout gut and skin microbiota. Journal of Animal Science and Biotechnology 12: 1-14. DOI: 10.1186/s40104-021-00551-9.
 
Tran, H.Q., Nguyen, T.T., Prokesova, M., Gebauer, T., Doan, H.V., Stejskal, V. 2022. Systematic review and meta- analysis of production performance of aquaculture species fed dietary insect meals. Reviews in Aquaculture 14: 1637- 1655. DOI:10.1111/raq.12666.
 
Valipour, M., Oujifard, A., Hosseini, A., Sotoudeh, E., Bagheri, D. 2019. Effects of dietary replacement of fishmeal by yellow mealworm (Tenebrio molitor) larvae meal on growth performance, hematological indices and some of non-specific immune responses of juvenile rainbow trout (Oncorhynchus mykiss). Iranian Scientific Fisheries Journal 28: 13-26. DOI: 20.1001.1.10261354.1398.28.2.10.3.
 
Wiegertjes, G.F., Stet, R.M., Parmentier, H.K., van Muiswinkel, W.B. 1996. Immunogenetics of disease resistance in fish: a comparative approach. Developmental and Comparative Immunology 20: 365-381. DOI: 10.1016/S0145-305X(96)00032-8.
 
Willora, F.P., Farris, N.W., Ghebre, E., Zatti, K., Bisa, S., Kiron, V., Verlhac-Trichet, V., Danielsen, M., Dalsgaard, T.K., Sørensen, M. 2025. Full-fat black soldier fly larvae meal and yellow mealworm meal: Impact on feed protein quality, growth and nutrient utilization of Atlantic salmon (Salmo salar) post smolts. Aquaculture 595: 741648. DOI: 10.1016/j.aquaculture.2024.741648.
 
Xia, W., Liu, P., Zhang, J., Chen, J. 2010. Biological activities of chitosan and chitooligosaccharides. Food Hydrocolloid 25: 170-179. DOI: 10.1016/j.foodhyd.2010.03.003.
Xu, G., Xing, W., Li, T., Xue, M., Ma, Z., Jiang, N., Luo, L. 2019. Comparative study on the effects of different feeding habits and diets on intestinal microbiota in Acipenser baeri Brandt and Huso huso. BMC Microbiology 19: 297. DOI: 10.1186/s12866-019-1673-6.
 
Zunzunegui, I., Martín-García, J., Santamaría, O., Poveda, J. 2024. Analysis of yellow mealworm (Tenebrio molitor) frass as a resource for a sustainable agriculture in the current context of insect farming industry growth. Journal of Cleaner Production 460: 142608. DOI: 10.1016/j.jclepro.2024.142608.