Mealworm (Tenebrio molitor) potencial in fish nutrition: a review

Authors

DOI:

https://doi.org/10.33448/rsd-v10i16.23229

Keywords:

Alternative protein fonts; Coleoptera; Fish meal; Insects; Production.

Abstract

The creation of aquatic organisms it is constantly growing and with this comes the need to meet this demand with the increased production of inputs such as feed for aquaculture. Fish nutrition is mainly characterized by the use of fish meal and oil for the manufacture of rations for their food. Soybean bran is the second most used ingredient as a source of protein in the production of feed for aquaculture. However, these ingredients compete with other feed segments, increasing cost or reducing market availability. Therefore, alternative sources of protein must be studied and developed to meet this demand. In this sense, insects present themselves as sources of high quality protein, in addition to fatty acids, vitamins and minerals. Although there is a problem with large-scale production to meet the demand of the feed market, the ease of breeding certain species of insects is capable of making this reality possible. Thus, insects can be a likely alternative protein source in fish feed, replacing conventional sources. This review aims to evaluate the inclusion of mealworm in the fish diet, in terms of performance and discuss the results obtained.

References

Achuba, F. I. & Osakwe, S. A. (2003). Petroleum – induced free radical toxicity in African catfish (Clarias gariepinus). Fish. Physiol. Biochem., 29, 97-103.

Aguilar-Miranda, E. D., López, M. G., Escamilla-Santana, C. & Barba De La Rosa, A.P. (2002). Characteristics of maize flour tortilla supplemented with ground Tenebrio molitor larvae, J. Agric. Food Chem., 50 (1): 192-195.

Barone, R. S. C. (2017). Feed is the main input for aquaculture production. Aquaculture assets. CNA Brazil. Year 3. Ed.13.

Barroso, F.G., de Haro, C., Sánchez-Muros, M-J., Venegas, E., Martínez-Sánchez, A. & Pérez-Bañón, C. (2014). The potential of various insect species for use as food for fish. Aquaculture 422–423, 193-201. https://doi.org/10.1016/j.aquaculture.2013.12.024

Basto, A., Matos, E. & Valente, L. M. P (2020). Nutritional value of different insect larvae meals as protein sources for European sea bass (Dicentrarchus labrax) juveniles. Aquaculture 521, 735085. https://doi.org/10.1016/j.aquaculture.2020.735085

Bednářová, M., Borkovcová, M., Mlček, J., Rop, O. & Zeman, L. (2013). Edible insects - species suitable for entomophagy under condition of Czech Republic. Acta Univ. Agric. Silvic. Mendel. Brun, 61, 587-593. https://doi.org/10.11118/actaun201361030587

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. Ital. J. Anim. Sci. 14 (4), 4170. https://doi.org/10.4081/ijas.2015.4170

Berggren, A., Jansson, A. & Low, M. (2019). Approaching ecological sustainability in the emerging insects-as-food industry. Trends Ecol. Evol. 34, 132-138. https://doi.org/10.1016/j.tree.2018.11.005

Beveridge, T. J. (1999). Structures of Gram-negative cell walls and their derived membrane vesicles. J. Bacteriol. 181, 4725–4733.

Bovera, F., Marono, S., Di Meo, C. Piccolo, G., Iannaccone, F. & Nizza, A. (2010). Effect of mannanoligosaccharides supplementation on caecal microbial activity of rabbits. Animal, 9, 1522-1527. Doi: 10.1017/S1751731110000558

Bovera, F., Loponte, R., Marono, S., Piccolo, G., Parisi, G., Iaconisi, V., Gasco, L. & Nizza, A. (2016). Use of Tenebrio molitor larvae meal as protein source inbroiler diet: effect on growth performance, nutrient digestibility, and carcass and meat traits. J. Anim. Sci. 94 (2), 639-647. http://dx.doi.org/10.2527/jas2015-9201

Celik, M., Diler, A. & Kuçukgulmez, A. (2005). A comparison of the proximate compositions and fatty acid profi les of zander (Sander lucioperca) from two different regions and climatic conditions. Food Chemistry, Champaign. 92(4):637-641.

Chemello, G., Renna, M., Caimi, C., Guerreiro, I., Oliva-Teles, A., Enes, P., Biasato, I., Schiavone, A., Gai, F. & Gasco, L. (2020). Partially Defatted Tenebrio molitor Larva Meal in Diets for Grow-Out Rainbow Trout, Oncorhynchus mykiss (Walbaum): Effects on Growth Performance, Diet Digestibility and Metabolic Responses. Animals, 10, 229. https://doi.org/10.3390/ani10020229

Choi, B. D., Wong, N. A. K. & Auh, J.-H. (2017). Defatting and sonication enhances protein extraction from edible insects. Korean J. Food Sci. Anim. Resour., 37, 955-961. Doi: 10.5851/kosfa.2017.37.6.955

Danulat, E. (1987). Digestibility of chitin in cod, Gadus morhua, in vivo. Helgolander Meeresuntersuch, 41, 425–436.

De Francesco, M., Parisi, G., Pérez-Sánchez, J., Gómez-Réqueni, P., Médale, F., Kaushik, S.J., Mecatti, M. & Poli, B.M. (2007). Effect of high-level fish meal replacement by plant proteins in gilthead sea bream (Sparus aurata) on growth and body/fillet quality traits. Aquac. Nutr. 13, 361-372. https://doi.org/10.1111/j.1365-2095.2007.00485.x

De Marco, M., Martínez, S., Hernandez, F., Madrid, J., Gai, F., Rotolo, L., Belforti, M., Bergero, D., Katz, H., Dabbou, S., Kovitvadhi, A., Zoccarato, I., Gasco, L. & Schiavone, A. (2015). Nutritional value of two insect meals (Tenebrio molitor and Hermetia illucens) for broiler chickens: apparent nutrient digestibility, apparent ileal amino acid digestibility and apparent metabolizable energy. Anim. Feed Sci. Technol. 209, 211-218. https://doi.org/10.1016/j.anifeedsci.2015.08.006

Deng, J., Mai, K., Chen. L., Mi, H. & Zhang, L. (2015). Effects of replacing soybean meal with rubber seed meal on growth, antioxi dant capacity, non-specific immune response, and resistance to Aeromonas hydrophila in tilapia (Oreochromis niloticus x O. aureus). Fish & Shellfish Immunology, 44, 436-444. https://doi.org/10.1016/j.fsi.2015.03.018

Dernekbaşi, S. (2012). Digestibility and Liver Fatty Acid Composition of Rainbow Trout (Oncorhynchus mykiss) Fed by Graded Levels of Canola Oil. Turkish Journal of Fisheries and Aquatic Sciences 12, 105-113. 10.4194/1303-2712-v12_1_13

Desvaux, M., Dumas, E., Chafsey, I. & Hebraud, M. (2006). Protein cell surface display in gram-positive bacteria: from single protein to macromolecularprotein structure. FEMS Microbiol. Lett. 256, 1–15, http://dx.doi.org/10.1111/j.1574-6968.2006.00122.x

Dijkstra, J.M., Grimholt, U. Leong, J., Koop, B.F. & Hashimoto, K. (2013). Analysis of class II MHC gene data in teleost fish genomes reveals the dispensability of the DM peptide loading system in most vertebrates. BMC Evol. Biol., 13, p. 260.

Dorval, J., Leblond, V. S. & Hontela, A. (2003). Oxidative stress and loss of cortisol secretion in adrenocortical cells of rainbow trout (Oncorhynchus mykiss) exposed in vitro to endosulfan, an organochlorine pesticide. Aquat. Toxicol., 63, 229-241. https://doi.org/10.1016/S0166-445X(02)00182-0

Esteban, M. A., Cuesta, A., Ortuño, J. & Meseguer, J. (2001). Immunomodulatory effects of dietary intake of chitin on gilthead seabream (Sparus aurata L.) innate immune system. Fish Shellfish Immunol., 11, 303-315. https://doi.org/10.1006/fsim.2000.0315

FAO (2013). Food and Agriculture Organization of the United Nations. Edible insects: future prospects for food and feed security. Fisheries and Aquaculture Department, Rome, 171p.

FAO (2020). The State of World Fisheries and Aquaculture 2020. Sustainability in action. Rome. https://doi.org/10.4060/ca9229en

Faramarzi, M., Jafaryan, H., Roozbehfar, R., Jafari, M., Rashidi, Y., & Biria, M. (2012). Influences of probiotic bacilli via bioencapsulated Daphnia magna on resistance of Persian sturgeon larvae against challenge tests. Glob Vet. 8 (4), 421-5.

Ferreira, M. S., Aride, P. H. R., Silva, M. N. P. & Val, A. L. (2013). Dietary protein and exercise training effects on the physiological and zootechnical parameters of matrinchã (Brycon amazonicus, Günther 1869). Acta Amazon. 43(4), 429-446.

Finke, M. D. (2002). Complete nutriente composition of commercially raised invertebrates used as food for insectivores. Zoo Biology, 21(3), 269-285.

Fontes, T. V., Oliveira, K. R. B., Almeida, I. L. G., Orlando, T. M., Rodrigues, P. B., Costa, D. V. & Rosa, P. V. (2019). Digestibility of Insect Meals for Nile Tilapia Fingerlings. Animals, 9, 181. https://doi.org/10.3390/ani9040181

Fraanje, W. & Garnett, T. (2020). Soy: food, feed, and land use change. (Foodsource: Building Blocks). Food Climate Research Network, University of Oxford. https://foodsource.org.uk/sites/default/files/building-blocks/pdfs/fcrn_building_block_-_soy_food_feed_and_land_use_change.pdf. Accessed on October 13, 2020.

García-Romero, J., Ginés, R., Izquierdo, M.S., Haroun, R., Badilla, R. & Rabaina, L. (2014). Effect of dietary substitution of fish meal for marine crab and echinoderm meals on growth performance, ammonia excretion, skin colour, and flesh quality and oxidation of red porgy (Pagrus pagrus). Aquaculture 422, 239-248. https://doi.org/10.1016/j.aquaculture.2013.11.024

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. Anim. Feed Sci. Technol., 220, 34-45. https://doi.org/10.1016/j.anifeedsci.2016.07.003

Gatlin, D. M., Barrows, F. T., Brown, P., Dabrowski, K., Gaylord, T. G., Hardy, R. W., Herman, E., Hu, G., Krogdahl, Å., Nelson, R., Overturf, K., Rust, M., Sealey, W., Skonberg, D., Souza, E. J., Stone, D., Wilson, R., & Wurtele, E. (2007). Expanding the utilization of sustainable plant products in aquafeeds: A review. Aquaculture Research, 38 (6), 551-579. https://doi.org/10.1111/j.1365-2109.2007.01704.x

Gause, B. R. & Trushenski, J. T. (2013). Sparing fish oil with beef tallow in feeds for rainbow trout: effects of inclusion rates and finishing on production performance and tissue fatty acid composition. N. Am. J. Aquacult. 75, 495-511. https://doi.org/10.1080/15222055.2013.811134

Geraylou, Z., Souffreau, C., Rurangwa, E., Maes, G. E., Spanier, K. I., Courtin, C. M., Delcour, J. A., Buyse, J., Ollevier, F. (2013). Prebiotic effects of arabinoxylan oligosaccharides on juvenile Siberian sturgeon (Acipenser baerii) with emphasis on the modulation of the gut microbiota using 454 pyrosequencing. FEMS Microbiol Ecol. 86 (2): 357-71. https://doi.org/10.1111/1574-6941.12169

Ghosh, S., Lee, S. M., Jung, C. & Meyer-Rochow, V. B. (2017). Nutritional composition of five commercial edible insects in South Korea. J. Asia-Pac. Entomol., 20, 686–694. https://doi.org/10.1016/j.aspen.2017.04.003

Glencross, B. D., Booth, M. & Allan, G. L. (2007). A feed is only as good as its ingredients – a review of ingredient evaluation strategies for aquaculture feeds. Aquac. Nutr. 13, 17-34. https://doi.org/10.1111/j.1365-2095.2007.00450.x

Gutowska, M. A., Drazen, J. C. & Robison, B. H. (2004). Digestive chitinolytic activity in marine fishes of Monterey Bay, California. Comp. Biochem. Physiol. 139A, 351–358.

Hardouin, J. & Mahoux, G., 2003. Zootechnie d’insectes – Elevage et utilisation au bénéfice de l'homme et de certains animaux. Bureau pour l’Echange et la Distribution de l’Information sur le Mini-élevage (BEDIM), 164 p.

Hasan, M. R. (2001). Nutrition and Feeding for Sustainable Aquaculture Development in the Third Millennium. In: Subasinghe, R.P., Bueno, P., Phillips, M.J., et al., Eds., Aquaculture in the Third Millennium. Technical Proceedings of the Conference on Aquaculture in the Third Millennium, Bangkok, Thailand, 20-25 February 2000. NACA, Bangkok and FAO, Rome, 193-219.

Heikkinen, J., Vielma, J., Kemiläinen, O., Tiirola, M., Eskelinen, P., Kiuru, T., Navia-Paldanius, D. & Von Wright, A. (2006). Effects of soybean meal based diet on growth performance, gut histopathology and intestinal microbiota of juvenile rainbow trout (Oncorhynchus mykiss). Aquaculture, 261, 259-268. https://doi.org/10.1016/j.aquaculture.2006.07.012

Henry, M. & Fountoulaki, E. (2014). Optimal dietary protein/lipid ratio for improved immune status of a newly cultivated Mediterranean fish species, the shi drum Umbrina cirrosa, L. Fish & Shellfish Immunology 37, 215–219. https://doi.org/10.1016/j.fsi.2014.02.005

Henry, M., Gasco, L., Piccolo, G. & Fountoulaki, E. (2015). Review on the use of insects in the diet of farmed fish: past and future. Anim. Feed Sci. Technol. 203, 1-22. https://doi.org/10.1016/j.anifeedsci.2015.03.001

Henry, M. A., Gai, F., Enes, P., Peréz-Jiménez, A. & Gasco, L. (2018a). Effect of partial dietary replacement of fishmeal by yellow mealworm (Tenebrio molitor) larvae meal on the innate immune response and intestinal antioxidant enzymes of rainbow trout (Oncorhynchus mykiss). Fish Shellfish Immunol. 83 , 308-313. https://doi.org/10.1016/j.fsi.2018.09.040

Henry, M. A., Gasco, L., Chatzifotis, S. & Piccolo, G. (2018b). Does dietary insect meal affect the fish immune system? The case of mealworm, Tenebrio molitor on European sea bass, Dicentrarchus labrax. Dev. Comp. Immunol. 81, 204-209. https://doi.org/10.1016/j.dci.2017.12.002

Hertrampf, J. W. & Piedade-Pascual, F. (2000). Handbook on Ingredients for Aquaculture Feeds. Kluwer Academic Publishers, Dordrecht, The Netherlands.

Hornung, B. (1991). The importance of mealworm larvae (Tenebrio molitor, L. 1758) as carriers of zearalenone when fed to insectivorous birds and other pet animals. In: Die Bedeutung der Larven des Mehlkafers (Tenebrio molitor, L. 1758) als Ubertrager von Zearalenon in der Futterung von insektivoren Vogeln und anderen Heimtieren. 81 pp.

Hua K. (2021). A meta-analysis of the effects of replacing fish meals with insect meals on growth performance of fish. Aquaculture 530, 735-732. https://doi.org/10.1016/j.aquaculture.2020.735732

Iaconisi, V., Marono, S., Parisi, G., Gasco, L., Genovese, L., Maricchiolo, G. & Piccolo, G. (2017). Dietary inclusion of Tenebrio molitor larvae meal: Effects on growth performance and final quality treats of blackspot sea bream (Pagellus bogaraveo). Aquaculture 476, 49-58. http://dx.doi.org/10.1016/j.aquaculture.2017.04.007

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. https://doi.org/10.1016/j.aquaculture.2017.11.034

Iaconisi, V., Secci, G., Sabatino, G., Piccolo, G., Gasco, L., Papini, A.M. & Parisi, G. (2019). Effect of mealworm (Tenebrio molitor L.) larvae meal on amino acid composition of gilthead sea bream (Sparus aurata L.) and rainbow trout (Oncorhynchus mykiss W.) fillets. Aquaculture 513, 734403. https://doi.org/10.1016/j.aquaculture.2019.734403

Ido, A., Hashizume, A., Ohta, T., Takahashi, T., Miura, C. & Miura, T. (2019). Replacement of fish meal by defatted yellow mealworm (Tenebrio molitor) larvae in diet improves growth performance and disease resistance in red seabream (Pargus major). Animals 9 (3), 100. https://doi.org/10.3390/ani9030100

Ikeda, M., Miyauchi, K. & Matsumiya, M. (2012). Purification and characterization of a 56 kDa chitinase isozyme (PaChiB) from the stomach of silver croaker Pennahia argentatus. Biosci. Biotechnol. Biochem., 76, 971-979. https://doi.org/10.1271/bbb.110989

Ikeda, M., Shirase, D., Sato, T., Ueda, M., Hirabayashi, S. & Matsumiya, M. (2014). Primary structure and enzymatic properties of chitinase isozymes purified from the stomach of the marbled rockfish Sebastiscus marmoratus. J. Chitin Chitosan Sci., 2, 106-116. https://doi.org/10.1166/jcc.2014.1048

IPIFF (2018). International Platform of Insects for Food and Feed (IPIFF). The European insect sector today: challenges, opportunities and regula tory landscape; IPIFF: Brussels, Belgium.

Iwasaki, A. & Medzhitov, R. (2010). Regulation of adaptive immunity by the innate immune system. Science 327, 291-295. Doi: 10.1126/science.1183021

Janssen, R. H., Vincken, J. P., van den Broek, L. A., Fogliano, V. & Lakemond, C. M. (2017). Nitrogen-to-protein conversion factors for three edible insects: Tenebrio molitor, Alphitobius diaperinus, and Hermetia illucens. J. Agric. Food Chem., 65, 2275-2278. Doi: 10.1021/acs.jafc.7b00471

Jeuniaux, C. (1993). Chitinolytic systems in the digestive tract of vertebrates: a review. Chitin Enzymol., 1 , 233-244.

Józefiak, A., Nogales-Mérida, S., Rawski, M., Kierończyk, B. & Mazurkiewicz, B. (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. https://doi.org/10.1186/s12917-019-2070-y

Junior, J. C. L., Ferreira, L. C. F. & Pederiva, K. A. (2018). Development of Tenebrio molitor L. larvae in different diets aiming at the production of insects for human consumption. Conection online (2018) n.18, ISSN 1980-7341.

Khan, S., Naz., Sultan, A., Alhidary, I. A., Abdelrahman, M. M., Khan, R. U., Khan, N. A., Khan, M. A. & Ahmad, S. (2016). Worm meal: a potential source of alternative protein in poultry feed. Poult. Sci. J., 72 (1), 93-102. https://dx.doi.org/10.1017/S0043933915002627

Khempaka, S., Chitsatchapong, C. & Molee, W. (2011). Effect of chitin and protein constituents in shrimp head meal on growth performance, nutrient digestibility, intestinal microbial populations, volatile fatty acids, and ammonia production in broilers. J. Appl. Poult. Res., 20, 1-11. https://doi.org/10.3382/japr.2010-00162

Khosravi, S., Kim, E., Lee, Y-S & Lee, S-M. (2018). Dietary inclusion of mealworm (Tenebrio molitor) meal as na alternative protein source in practical diets for juvenile rockfish (Sebastes schlegeli). Entomological Research 48, 214–221. https://doi.org/10.1111/1748-5967.12306

Kiron, V. (2012). Fish immune system and its nutritional modulation for preventive health care, Anim. Feed Sci. Technol. 173, 111-133. https://doi.org/10.1016/j.anifeedsci.2011.12.015

Klunder, H.C., Wolkers-Rooijackers, J., Korpela, J. M. & Nout, M. J. (2012). Microbiological aspects of processing and storage of edible insects. Food Control 26:628–31.

König, E., Bininda‐Emonds, R. P. & Shaw, C. (2015). The diversity and evolution of anuran skin peptides. Peptides 63, 96‐117. https://doi.org/10.1016/j.peptides.2014.11.003

Köprücü, K. & Özdemir, Y. (2005). Apparent digestibility of selected feed ingredients for Nile tilapia (Oreochromis niloticus). Aquaculture 250, 308-316. https://doi.org/10.1016/j.aquaculture.2004.12.003

Kroeckel, S., Harjes, A. G. E., Roth, I., Katz, H., Wuertz, S., Susenbeth, A. & Schulz, C. (2012). When a turbot catches a fly: evaluation of a pre-pupae meal of the Black Soldier Fly (Hermetia illucens) as fish meal substitute - growth performance and chitin degradation in juvenile turbot (Psetta maxima). Aquaculture, v. 364-365, 345-352. https://doi.org/10.1016/j.aquaculture.2012.08.041

Krogdahl, Å., Hemre, G. I. & Mommsen, T. P. (2005). Carbohydrates in fish nutrition: Digestion and absorption in postlarval stages. Aquac. Nutr., 11, 103-122.

Kurokawa, T., Uji, S. & Suzuki, T. (2004). Molecular cloning of multiple chitinase genes in Japanese flounder Paralichthys olivaceus. Comp. Biochem. Physiol. B: Biochem. Mol. Biol., 138, 255-264. https://doi.org/10.1016/j.cbpc.2004.03.015

Kurtz, J. Kalbe, M., Aeschlimann, P. B., Haberli, M. A., Wegner, K. M., Reusch, T. B. H. & Milinski, M. (2004). The diversity of the major histocompatibility complex influences the parasite resistance and innate immunity in sticklebacks. P. Roy. Soc. B-Biol. Sci., 271, pp. 197 – 204. https://doi.org/10.1098/rspb.2005.3450

Kus, M. M. & Mancini-Filho, J. (2010). Fatty Acids: Eicosapentaenoic (EPA) and Docosahexaenoic (DHA). Series of Publications Ilsi Brasil: Fully Recognized Functions of Nutrients, vol. 17, p. 1-20.

Lee, C. G., Da Silva, C.A., Lee, J.-Y., Hartl, D. & Elias, J.A. (2008). Chitin regulation of imune responses: an old molecule with new roles. Curr. Opin. Immunol. 20, 684-689. https://doi.org/10.1016/j.coi.2008.10.002

Lenaerts, S., Van Der Borght, M., Callens, A. & Van Campenhout, L. (2018). Suitability of microwave drying for mealworms (Tenebrio molitor) as alternative to freeze drying: Impact on nutritional quality and colour. Food Chem., 254, 129–136. https://doi.org/10.1016/j.foodchem.2018.02.006

Li, F. W., Wang, W. L., Li, E. X., Li, S. Y. & Liu, C. A. (2008). Analysis of fatty acids in Tenebrio molitor linneeus by GC‐US. Food Research & Development 29, 92-94.

Lie, Ø. (2001). Flesh quality – the role of nutrition. Aquaculture Research. 32, 341-348. https://doi.org/10.1046/j.1355-557x.2001.00026.x

Lin, D., Mao, Y. & Cai, F. (1990). Nutritional lipid liver disease of grass carp Ctenopharyngodon idullus (C. et V.). Chin. J. Oceanol. Limn., 8, 363-373.

Liu, W. X., Wei, M. C. & Liu, G. Q. (2005). Bioactive compounds from insects and its development perspective. Food Sci. Technol. 1, 48-51.

Liu, Y. S., Wang, F. B., Cui, J. X. & Zhang, L. (2010). Recent status and advances on study and utilization of Tenebrio molitor. Journal of Environmental Entomology 32, 106-114.

Loponte, R., Marono, S., Iaconisi, V., Piccolo, G., Parisi, G. & Bovera, F. (2016). Caecal volatile fatty acid production of broilers fed Tenebrio molitor larvae meal. INSECTA 2016 International Symposium on Insects as Food, Feed and Non-Food, Magdeburg (Germany), 12th September 2016.

Magnadóttir, B. (1998). Comparison of immunoglobulin (IgM) from four fish species. Icel. Agr. Sci., 12, 47-59.

Maehre, H. K., Dalheim, L., Edvinsen, G. K., Elvevoll, E. O. & Jensen, I. J. (2018). Protein determination - method matters. Foods 7(1), 5. https://doi.org/10.3390/foods7010005

Makkar, H. P. S., Tran, G., Heuzé, V. & Ankers, P. (2014). Rewiew: State-of-the-art on use of insects as animal feed. Anim. Feed Sci. Technol., 197, 1-33. https://doi.org/10.1016/j.anifeedsci.2014.07.008

Marono, S., Piccolo, G., Loponte, R., Di Meo, C., Attia, Y. A., Nizza, A. & Bovera, F. (2015). In vitro crude protein digestibility of Tenebrio molitor and Hermetia illucens insect meals and its correlation with chemical composition traits. Ital. J. Anim. Sci. 14, 3889. https://doi.org/10.4081/ijas.2015.3889

Megido, R. C., Desmedt, S., Blecker, C., Béra, F., Haubruge, E., Alabi, T. & Francis, F. (2017). Microbiological load of edible insects found in Belgium. Insects 8:12.

Menezes, M. E. S., Lira, G. M., Omena, C. M. B., Freitas, J. D. & Sant’Ana, A. E. G. (2009). Nutritive values of fishes from maritime coast of Alagoas, Brazil. Rev. Inst. Adolfo Lutz (Impr.) [online], vol.68, n.1 [citado 2021-08-11], pp. 21-28.

Menezes, C. W. G., Camilo, S. S., Fonseca, A. J., Júnior, S. L. A., Bispo, D. F. & Soares, M. A. (2014). Can the diet of the prey Tenebrio molitor (Coleoptera: Tenebrionidae) affect the development of the predator Podisus nigrispinus (Heteroptera: Pentatomidae)? Arq. Inst. Biol., 81, 3, 250-256. https://doi.org/10.1590/1808-1657001212012

Mohieldein, A., Hyder, M. A. & Hasan, M. (2013). Comparative levels of ALT, AST, ALP and GGT in liver associated diseases. Eur. J. Exp. Biol., 3 (2), 280-284.

Mroz, Z. (2005). Organic acids as potential alternatives to antibiotic growth promoters for pigs. Adv. Pork Prod. 16, 169–182.

Munshi J. S. D. & Dutta H. M. (1996). Fish Morphology: Horizon of New Research. Science Publishers, 300p.

Nascimento, A. C., Fontes, W., Sebben, A. & Castro, M. S. (2003). Antimicrobial peptides from anurans skin secretions. Protein Pept Lett., 10 (3), 227-238.

Navarre, W. W. & Schneewind, O. (1999). Surface proteins of gram-positive bacteria and mechanisms of their targeting to the cell wall envelope. Microbiol.Mol. Biol. Rev. 63, 174–229.

Nawrocki, K. L., Crispell, E. K. & McBride, S. M. (2014). Antimicrobial peptide resistance mechanisms of Gram-positive bacteria. Antibiotics, 3 (4), 461-492. https://doi.org/10.3390/antibiotics3040461

New, M. B. & Wijkstroem, U. N. (2002). Use of Fishmeal and Fish Oil in Aquafeeds: Further Thoughts on the Fishmeal Trap. FAO Fisheries Circular No. 975.

Ngo, D. H. & Kim, S. K. (2014). Antioxidant effects of chitin, chitosan, and their derivatives. Adv. Food Nutr. Res. 73, 15-31. https://doi.org/10.1016/B978-0-12-800268-1.00002-0

NRC (2011). Nutrient Requirements of Fish and Shrimp, 1st ed. (Washington, DC, USA).

OECD/FAO (2019). OECD-FAO Agricultural Outlook 2019-2028, OECD Publishing, Paris/Food and Agriculture Organization of the United Nations, Rome. https://doi.org/10.1787/agr_outlook-2019-en

Parra, J. R. P. (2009). The evolution of artificial diets and their interactions in science and technology. In: Panizzi, A.R. & Parra, J.P.R. (Ed). Insect bioecology and nutrition: basis for integrated pest management. Embrapa: Brasília, p.91-174.

Piccolo, G., Marono, S., Gasco, L., Iannaccone, F., Bovera, F. & Nizza, A. (2014). Use of Tenebrio molitor larvae meal in diets for Gilthead seabream (Sparus aurata) juveniles. Insects to Feed The World (p. 76). The Netherlands: Wageningen University.

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. https://doi.org/10.1016/j.anifeedsci.2017.02.007

Ramos-Elorduy, J., González, E.A., Hernández, A. R. & Pino, J. M. (2002). Use of Tenebrio molitor (Coleoptera: Tenebrionidae) to recycle organic wastes and as feed for broiler chickens. J. Econ. Entomol. 95 (1), 214-220. https://doi.org/10.1603/0022-0493-95.1.214

Ramos Filho, M. M., Ramos, M. I. L., Hiane, P. A. & Souza, E. M. T. (2008). Perfi lipídico de quatro espécies de peixes da região pantaneira de Mato Grosso do Sul. Ciênc. Tecnol. Aliment., Campinas., 28(2): 361-5

Rauta, P. R., Nayak, B. & Das, S. (2012). Immune system and immune responses in fish and their role in comparative immunity study: a model for higher organisms. Immunol. Lett. 148 (1), 23-33. https://doi.org/10.1016/j.imlet.2012.08.003

Rema, P., Saravanan, S., Armenjon, B, Motte, C. & Dias, J. (2019). Graded incorporation of defatted yellow mealworm (Tenebrio molitor) in rainbow Trout (Oncorhynchus mykiss) diet improves growth performance and nutrient retention. Animals, 9, 187. doi:10.3390/ani9040187

Ribeiro, G.O. (2019). Flour from the larvae of Tenebrio molitor in the feeding of Nile tilapia. Thesis (Master's degree). Postgraduate Program in Animal Science, State University of Montes Claros (Unimontes), Minas Gerais, MG.

Ringø, E., Zhou, Z., Vecino, J. L. G., Wadsworth, S., Romero, J., Krogdahl, Å., Olsen, R. E., Dimitroglou, A., Foey, A., Davies, S., Owen, M., Lauzon, H. L., Martinsen, P., De Schryver, P., Bossier, P., Sperstad, S. & Merrifield, D. L. (2015). Effect of dietary components on the gut microbiota of aquatic animals. A never- ending story? Aquaculture Nutrition 22, 219-282. http://dx.doi.org/10.1111/anu.12346

Rumpold, B. A. & Schlüter, O. K. (2013). Potential and challenges of insects as an innovative source for food and feed production. Innov. Food Sci. Emerg. Technol. 17, 1-11. https://doi.org/10.1016/j.ifset.2012.11.005

Sakai, M., Kamiya, H., Ishii, S., Atsuta, S. & Kobayashi, M. (1992). The immunostimulating effects of chitin in rainbow trout, Oncorhynchus mykiss. Dis. Asian Aquacult., 1, 413-417.

Sales, J. & Janssens, G. P. J. (2003). Nutrient requirements of ornamental fish. Aquat. Living Resour. 16, 533-540. Doi:10.1016/j.aquliv.2003.06.001

Sánchez, T. C. I. & Burgos, Y. V. (2014). Determination of anthocyanins and nutritional value of tenebrios (Tenebrio molitor) fed with diets enriched with maize maize (Zea mays L.). Course Conclusion Paper (Biotechnology Engineering of Natural Resources). Universidad Politécnica Salesiana Sede Quito - Quito, Ecuador.

Sánchez-Muros, M.J., Barroso, F. G. & Manzano-Agugliaro, F. (2014). Insect meal as renewable source of food for animal feeding: a review. J. Clean. Prod. 65, 16-27.

Sánchez-Muros, J., de Haro, C., Sanz, A., Trenzado, C. E., Villareces, S. & Barroso, F. G. (2015). Nutritional evaluation of Tenebrio molitor meal as fishmeal substitute for tilapia (Oreochromis niloticus) diet. Aquaculture Nutrition 22, 943-955.

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. https://doi.org/10.1016/j.aquaculture.2018.07.012

Saurabh, S. & Sahoo, P. K. (2008). Lysozyme: an important defence molecule of fish innate immune system. Aquac. Res., 39, 223-239.

Sealey, W. M., Gaylord, T. G., Barrows, F. T., Tomberlin, J. K., McGuire, M. A., Ross, C. & St-Hilaire, S. (2011). Sensory analysis of rainbow trout, Oncorhynchus mykiss, fed enriched Black Soldier Fly prepupae, Hermetia illucens. J. World Aquacult. Soc. 42, 34-45. https://doi.org/10.1111/j.1749-7345.2010.00441.x

Skalli, A. & Robin, J. H. (2004). Requirement of n-3 long chain polyunsaturated fatty acids for European sea bass (Dicentrarchus labrax) juveniles: growth andfatty acid composition. Aquaculture 240, 399-415, http://dx.doi.org/10.1016/j.aquaculture.2004.06.036.

Song, S. G., Chi, S. Y., Tan, B. P., Liang, G. L., Lu, B. Q., Dong, X. H., Yang, Q. H., Liu, H. Y & Zhang, S. (2018). Effects of fishmeal replacement by Tenebrio molitor meal on growth performance, antioxidante enzyme activities and disease resistance of the juvenile pearl gentian grouper (Epinephelus lanceolatus x Epinephelus fuscoguttatus). Aquaculture Research, 49, 2210-2217. https://doi.org/10.1111/are.13677

Souza, P. C. & Teles, B. R. (2011). Life cycle of Tenebrio molitor (Coleoptera) larvae, under different diets. IN: Proceedings of the XX Scientific Initiation Day PIBIC INPA - CNPq / FAPEAM, Manaus.

Spang, B. (2013). Insects as food: assessing the food conversion efficiency of the mealworm (Tenebrio Molitor). Environmental study master thesis: The Evergreen State College.

Sperandio LM. A Importância do Peixe na Alimentação Humana. GO. Disponível em <http://www.setorpesqueiro.com.br/portal. asp.

Stansby, M. E. (1973). Polynsaturates and fat in fi sh fl esh. J. Am. Diet. Ass., 63: 625-30.

St-Hilaire, S., Sheppard, C., Tomberlin, J. K., Irving, S., Newton, L., McGuire M. A., Mosley, E. E., Hardy, E. E., Hardy, R. W. & Sealey, W. (2007). Fly prepupae as a feedstuff for rainbow trout, Oncorhynchus mykiss. J. World Aquacult. Soc. 38, 59-67. https://doi.org/10.1111/j.1749-7345.2006.00073.x

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 Shellfish Imm., 69, 59-66. https://doi.org/10.1016/j.fsi.2017.08.008

Superior Health Council (2014). Food safety aspects of insects intended for human consumption. Scientific Committee of the Federal Agency for the safety of food Chain, 9160, 1-23.

Tacon, A. G. J., Hasan, M. R., Allan, G., El-Sayed, A. -F., Jackson, A., Kaushik, S. J., Ng, W-K., Suresh, V. & Viana, M. T. (2012). Aquaculture feeds: addressing the longterm sustainability of the sector. In: Subasinghe, R. P., Arthur, J. R., Bartley, D. M., De Silva, S. S., Halwart, M., Hishamunda, N., Mohan., C. V & Sorgeloos, P. Eds. Farming the Waters for People and Food. Proceedings of the Global Conference on Aquaculture 2010, Phuket, Thailand. 22-25 September 2010. pp. 193-231. FAO, Rome and NACA, Bangkok.

Teh, S.-S., Bekhit, A.E.-D., Carne, A. & Birch, J. (2013). Effect of the defatting process, acid and alkali extraction on the physicochemical and functional properties of hemp, flax and canola seed cake protein isolates. J. Food Measure. Charact., 8 (2013), pp. 92-104, 10.1007/s11694-013-9168-x

Tharanathan, R. N. & Kittur, F. S. (2003). Chitin – The undisputed biomolecule of great potential. Crit. Rev. Food Sci. Nutr., 43, 61–87.

Tibaldi, E., Zittelli, G. C., Parisi, G., Bruno, M., Giorgi, G., Tulli, F., Venturini, S., Tredici, M. R. & Poli, B. M. (2015). Growth performance and quality traits of European sea bass (D. labrax) fed diets including increasing levels of freeze-dried Isochrysis sp. (T-ISO) biomass as a source of protein and n-3 long chain PUFA in partial substitution of fish derivatives. Aquaculture 440, 60-68. https://doi.org/10.1016/j.aquaculture.2015.02.002

Tubin, J. S. B., Paiano, D., Hashimotob, G. S. O., Furtado, W. E., Martins, M. L, Durigon, E. & Emerenciano, M. G. C. (2020). Tenebrio molitor meal in diets for Nile tilapia juveniles reared in biofloc system. Aquaculture 519, 734-763. https://doi.org/10.1016/j.aquaculture.2019.734763

United Soybean Board (2019). Supply & Disappearance. USB Market View Database (n.d.). Available at: https://marketviewdb.centrec.com/sd/. (Accessed: 2nd August 2020)

van Broekhoven, S., Oonincx, D. G. A. B., van Huis, A., van Loon, J. J. A. (2015) Growth performance and feed conversion efficiency of three edible mealworm species (Coleoptera: Tenebrionidae) on diets composed of organic by-products J. Insect Physiol. 73, 1-10. https://doi.org/10.1016/j.jinsphys.2014.12.005

Veldkamp, T., van Duinkerken, G., van Huis, A., Lakemond, C. M. M, Ottevanger, E., Bosch, G. & van Boekel, T. (2012). Insects as a sustainable feed ingredient in pig and poultry diets: a feasibility study. Wageningen UR Livestock Production, report 638, p.1-48.

Veldkamp, T. & Bosch, G. (2015). Insects: um ingrediente rico em proteínas na dieta de suínos e aves. Anim Front., 5: 45–50.

Vilella, L. M. (2018). Production of insects for use in animal feed. Course Conclusion Paper (Zootechnics), Faculty of Agronomy, Federal University of Rio Grande do Sul (UFRGS), Porto Alegre, RS.

Zasloff, M. (2002). Antimicrobial peptides of multicellular organisms. Nature 415, 389-395.

Zoccarato, I., Benatti, G., Bianchini, M. L., Boccignogne, M., Conti, A., Napolitano, R. & Palmegiano, G. B. (1994). Differences in performances, flesh composition and water output quality in relation to density and feeding levels in rainbow trout Oncorhynchus mykiss (Walbaum) farming. Aquac. Fish. Manag. 25, 639-647. https://doi.org/10.1111/j.1365-2109.1994.tb00728.x

Zhu, L-Y., Nie, L., Zhu, G., Xiang, L-X. & Shao, J-Z. (2013). Advances in research of fish immune-relevant genes: a comparative overview of innate and adaptive immunity in teleosts. Dev. Comp. Immunol. 39, 39-62. https://doi.org/10.1016/j.dci.2012.04.001

Downloads

Published

12/12/2021

How to Cite

LIMA, J. S. de .; PITTALUGA, M. L. .; LOVATTO, N. de M. .; VEIVERBERG, C. A.; BORILLE, R.; LAZZARI, R. Mealworm (Tenebrio molitor) potencial in fish nutrition: a review. Research, Society and Development, [S. l.], v. 10, n. 16, p. e269101623229, 2021. DOI: 10.33448/rsd-v10i16.23229. Disponível em: https://rsdjournal.org/index.php/rsd/article/view/23229. Acesso em: 26 apr. 2024.

Issue

Section

Review Article