Dietary Inclusion of Tenebrio Molitor Meal in Sea Trout Larvae Rearing: Effects on Fish Growth Performance, Survival, Condition, and GIT and Liver Enzymatic Activity

Aksnes A., Hope B., Jönsson E., Björnsson B.T., Albrektsen S. (2006). Size-fractionated fish hydrolysate as feed ingredient for rainbow trout (Oncorhynchus mykiss) fed high plant protein diets. I. Growth, growth regulation and feed utilization. Aquaculture, 261: 305–317.10.1016/j.aquaculture.2006.07.025Search in Google Scholar

Alp A., Erer M., Kamalak A. (2010). Eggs incubation, early development, and growth in fry of brown trout (Salmo trutta macrostigma) and black sea trout (Salmo trutta labrax). Turkish J. Fish. Aquat. Sci., 10: 387–394.Search in Google Scholar

Antonopoulou E., Nikouli E., Piccolo G., Gasco L., Gai F., Chatzifotis S., Men-te E., Kormas K.A. (2019). Reshaping gut bacterial communities after dietary Tenebrio molitor larvae meal supplementation in three fish species. Aquaculture, 503: 628–635.10.1016/j.aquaculture.2018.12.013Search in Google Scholar

Arzel J., Mctailler R., Kerleguer C., Le Delliou H., Guillaume J. (1995). The protein requirement of brown trout (Salmo trutta) fry. Aquaculture, 130: 67–78.10.1016/0044-8486(94)00201-XSearch in Google Scholar

Azarm H.M., Kenari A.A., Hedayati M. (2013). Effect of dietary phospholipid sources and levels on growth performance, enzymes activity, cholecystokinin and lipoprotein fractions of rainbow trout (Oncorhynchus mykiss) fry. Aquacult. Res., 44: 634–644.10.1111/j.1365-2109.2011.03068.xSearch in Google Scholar

Baeverfjord G., Krogdahl A. (1996). Development and regression of soybean meal induced enteritis in Atlantic salmon, Salmo salar L., distal intestine: a comparison with the intestines of fasted fish. J. Fish Dis., 19: 375–38710.1111/j.1365-2761.1996.tb00376.xSearch in Google Scholar

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: 670–676.10.4081/ijas.2015.4170Search in Google Scholar

Chalamaiah M., Kumar B.D., Hemalatha R., Jyothirmayi T. (2012). Fish protein hydrolysates: Proximate composition, amino acid composition, antioxidant activities and applications: A review. Food Chem., 135: 3020–3038.10.1016/j.foodchem.2012.06.100Search in Google Scholar

CITES,UNEP-WCMC. (2017). The Checklist of CITES Species Website. Appendices I, II and III valid from 04 April 2017. CITES Secretariat, Geneva, Switzerland. Compiled by UNEP-WCMC, Cambridge, UK.Search in Google Scholar

Cowey C.B., Sargent J.R. (1972). Fish nutrition. Adv. Mar. Biol., 10: 383–494.10.1016/S0065-2881(08)60419-8Search in Google Scholar

Dąbrowski K., Poczyczynski P., Köck B., Berger B. (1989). Effect of partially or totally replacing fish meal protein by soybean meal protein on growth, food utilization and proteolytic enzyme activities in rainbow trout (Salmo gairdneri). New in vivo test for exocrine pancreatic secretion. Aquaculture, 77: 29–49.10.1016/0044-8486(89)90019-7Search in Google Scholar

Domagała J., Dziewulska K., Czerniawski R. (2014). Survival rate and growth in the wild of sea trout (Salmo trutta L.) fry obtained using frozen semen. Arch. Pol. Fish., 22: 265–270.10.2478/aopf-2014-0028Search in Google Scholar

FAO (2016). The state of world fisheries and aquaculture. Contributing to food security and nutrition for all. Rome, Italy 200 pp.Search in Google Scholar

FAO (2018). The state of world fisheries and aquaculture, meeting the sustainable development goals. Rome, Italy 210 pp.Search in Google Scholar

Farhangi M., Carter C.G. (2001). Growth, physiological and immunological responses of rainbow trout (Oncorhynchus mykiss) to different dietary inclusion levels of dehulled lupin (Lupinus angustifolius). Aquacult. Res. 32 (Suppl. 1): 329–340.10.1046/j.1355-557x.2001.00044.xSearch in Google Scholar

Fasakin E.A., Balogun A.M., Ajayi O.O. (2003). Evaluation of full-fat and defatted maggot meals in the feeding of clariid catfish Clarias gariepinus fingerlings. Aquacult. Res., 34: 733–738.10.1046/j.1365-2109.2003.00876.xSearch in Google Scholar

Fearnside P.M. (2001). Soybean cultivation as a threat to the environment in Brazil. Environ. Conserv., 28: 23–38.10.1017/S0376892901000030Search in Google Scholar

Fraser D.J. (2008). How well can captive breeding programs conserve biodiversity? A review of salmonids. Evol. Appl. 1: 535–586.10.1111/j.1752-4571.2008.00036.xSearch in Google Scholar

Freeman M.C., Pringle C.M., Greathouse E.A., Freeman B.J. (2003). Ecosystem-level consequences of migratory faunal depletion caused by dams. In: Biodiversity, status, and conservation of the world’s shads, Limburg K.E., Waldman J.R. (eds). American Fisheries Society, Symposium Bethesda, Maryland, 35: 255–266.Search in Google Scholar

Frøystad M.K., Lilleeng E., Sundby A., Krogdahl A. (2006). Cloning and characterization of alpha-amylase from Atlantic salmon (Salmo salar L.). Comp. Biochem. Physiol. A Mol. Integr. Physiol., 45: 479–492.10.1016/j.cbpa.2006.08.003Search in Google Scholar

Furné M., Hidalgo M.C., López A., García-Gallego M., Morales A.E., Domezai-né J., Sanz A. (2005). Digestive enzyme activities in Adriatic sturgeon Acipenser naccarii and rainbow trout Oncorhynchus mykiss. A comparative study. Aquaculture, 250: 391–398.10.1016/j.aquaculture.2005.05.017Search in Google Scholar

Furné M., García-Gallego M., Hidalgo M.C., Morales A.E., Domezain A., Do-mezain J., Sanz A. (2008). Effect of starvation and refeeding on digestive enzyme activities in sturgeon (Acipenser naccarii) and trout (Oncorhynchus mykiss). Comp. Biochem. Physiol. A Mol. Integr. Physiol., 149: 420–425.10.1016/j.cbpa.2008.02.002Search in Google Scholar

Gasco L., Henry M., Piccolo G., Marono S., Gai F., Renna M., Lussiana C., Anto-nopoulou 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: 34–45.10.1016/j.anifeedsci.2016.07.003Search in Google Scholar

Gilbert E.R., Wong E.A., Webb K.E. (2008). Board-invited review: Peptide absorption and utilization: Implications for animal nutrition and health. J. Anim. Sci., 86: 2135–2155.10.2527/jas.2007-0826Search in Google Scholar

Gildberg A., Johansen A., Bøgwald J. (1995). Growth and survival of Atlantic salmon (Salmo salar) fry given diets supplemented with fish protein hydrolysate and lactic acid bacteria during a challenge trial with Aeromonas salmonicida. Aquaculture, 138: 23–34.10.1016/0044-8486(95)01144-7Search in Google Scholar

González J.D., Caballero A., Viegas I., Metón I., Jones J.G., Barra J., Fernán-dez F., Baanante I.V. (2012). Effects of alanine aminotransferase inhibition on the intermediary metabolism in Sparus aurata through dietary amino-oxyacetate supplementation. Br. J. Nutr., 107: 1747–1756.10.1017/S000711451100496XSearch in Google Scholar

Hamre K., Yúfera M., Rønnestad Boglione C., Conceição L.E.C., Izquierdo M. (2013). Fish larval nutrition and feed formulation: knowledge gaps and bottlenecks for advances in larval rearing. Rev. Aquacult., 4: 526–558.10.1111/j.1753-5131.2012.01086.xSearch in Google Scholar

Hansen T. (1985). Artificial hatching substrate: effect on yolk absorption, mortality and growth during first feeding of sea trout (Salmo trutta). Aquaculture, 46: 275–285.10.1016/0044-8486(85)90105-XSearch in Google Scholar

Hardy R.W., Barrows F.T. (2002). Diet formulation and manufacture. In: Fish Nutrition, Hal- ver J.E., Hardy R.W. (eds). 3rd ed. Academic Press Inc., San Diego, CA, USA, pp. 506–601.Search in Google Scholar

Hasan M.R. (2001). Nutrition and feeding for sustainable aquaculture development in the third millennium. In: Aquaculture in the Third Millennium, Subasinghe R.P., Bueno P., Phillip M.J., Hough C., McGladdery S.E., Arthur J.R. (eds). Technical Proceedings of the Conference on Aquaculture in the Third Millennium, Bangkok, Thailand, 20-25 February 2000. NACA, Bangkok and FAO, Rome, pp. 193–219.Search in Google Scholar

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: 1–22.10.1016/j.anifeedsci.2015.03.001Search in Google Scholar

Hevrøy E.M., Espe M., Waagbø R., Sandnes K., Ruud M., Hemre G.-I. (2005). Nutrient utilization in Atlantic salmon (Salmo salar L.) fed increased levels of fish protein hydrolysate during a period of fast growth. Aquacult. Nutr., 11: 301–313.10.1111/j.1365-2095.2005.00357.xSearch in Google Scholar

Hidalgo M.C., Urea E., Sanz A. (1999). Comparative study of digestive enzymes in fish with different nutritional habits. Proteolytic and amylase activities. Aquaculture, 170: 267–283.10.1016/S0044-8486(98)00413-XSearch in Google Scholar

Hull R., Katete R., Ntwasa M. (2012). Therapeutic potential of antimicrobial peptides from insects. Biotechnol. Mol. Biol. Rev., 7: 31–47.Search in Google Scholar

Iaconisi V., Marono S., Parisi G., Gasco L., Genovese L., Maricchiolo G., Bove-ra F., 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: 49–58.10.1016/j.aquaculture.2017.04.007Search in Google Scholar

Kaushik S.J., Cravedi J.P., Lalles J.P., Sumpter J., Fauconneau B., Laroche M. (1995). Partial or total replacement of fish meal by soybean protein on growth, protein utilization, potential estrogenic or antigenic effects, cholesterolemia and flesh quality in rainbow trout, Oncorhynchus mykiss. Aquaculture, 133: 257–274.10.1016/0044-8486(94)00403-BSearch in Google Scholar

Krogdahl A., Lea T.B., Olli J.J. (1994). Soybean proteinase inhibitors affect intestinal trypsin activities and amino-acid digestibilities in rainbow trout (Oncorhynchus mykiss). Comparative Biochemistry and Physiology Part A: Physiology, 107: 215–219.10.1016/0300-9629(94)90296-8Search in Google Scholar

Krogdahl Å., Hemre G-I., Mommsen T.P. (1999). Carbohydrates in fish nutrition: digestion and absorption in postlarval stages. Aquacult. Nutr., 11: 103–122.10.1111/j.1365-2095.2004.00327.xSearch in Google Scholar

Le Féon S., Thévenot A., Maillard F., Macombe C., Forteau L., Aubin J. (2019). Life cycle assessment of fish fed with insect meal: Case study of mealworm inclusion in trout feed, in France. Aquaculture, 500: 82–91.10.1016/j.aquaculture.2018.06.051Search in Google Scholar

Leary S., Underwood W., Anthony R., Cartner S., Corey D., Grandin T., Greena-cre C., Gwaltney-Brant S., Mc Crackin M.A., Meyer R., Miller D., Shearer J., Yanong R. (2013). AVMA guidelines for the euthanasia of animals: 2013 edition, pp. 32.Search in Google Scholar

Li Q., Zheng L., Qiu N., Cai H., Tomberlin J.K., Yu Z. (2011). Bioconversion of dairy manure by black soldier fly (Diptera: Stratiomyidae) for biodiesel and sugar production. Waste Manage., 31: 1316–1320.10.1016/j.wasman.2011.01.005Search in Google Scholar

Martin S.A.M., Vilhelmsson O., Médale F., Watt P., Kaushik S., Houlihan D.F. (2003). Proteomic sensitivity to dietary manipulations in rainbow trout. Biochim. Biophys. Acta – Proteins and Proteomics, 1651: 17–29.10.1016/S1570-9639(03)00231-0Search in Google Scholar

Minh N.P. (2015). Alcalase and protamex hydrolysis of bioactive peptides from soybean. Bull. Environ. Pharmacol. Life Sci., 4: 132–143.Search in Google Scholar

Murray A.L., Pascho R.J.Alcorn S.W., Fairgrieve W.T., Shearer K.D., Roley D. (2003). Effects of various feed supplements containing fish protein hydrolysate or fish processing by-products on the innate immune functions of juvenile coho salmon (Oncorhynchus kisutch). Aquaculture, 220: 643–653.10.1016/S0044-8486(02)00426-XSearch in Google Scholar

Muzzarelli R.A.A. (2010). Chitins and chitosans as immunoadjuvants and non-allergenic drug carriers. Mar. Drugs, 8: 292–312.10.3390/md8020292Search in Google Scholar

Ng W.-K., Liew F.-L., Ang L.-P., Wong K.-W. (2001). Potential of mealworm (Tenebrio molitor) as an alternative protein source in practical diets for African catfish, Clarias gariepinus. Aquacult. Res., 32 (Suppl. 1): 273–280.10.1046/j.1355-557x.2001.00024.xSearch in Google Scholar

NRC, National Research Council (1981). Nutrient requirements of coldwater fishes (Nutrient requirements of domestic animals). National Academy Press, Washington DC.Search in Google Scholar

NRC, National Research Council (1993). Nutrient Requirements of Fish. Washington, DC: The National Academies Press.Search in Google Scholar

Oonincx D.G.A.B, van Itterbeeck J., Heetkamp M.J.W., vanden Brand H., van Loon J.J.A., van Huis A. (2010). An exploration on greenhouse gas and ammonia production by insect species suitable for animal or human consumption. PLoS One, DOI:10.1371/journal. pone.0014445.10.1371/journal.pone.0014445Search in Google Scholar

Ovissipour M., Benjakul S., Safari R., Motamedzadegan A. (2010). Fish protein hydrolysates production from fin tuna Thunnus albacares head using Alcalase and Protamex. Intern. Aqua. Res., 2: 87–95.Search in Google Scholar

Pasupuleti V.K., Braun S. (2010). State of the Art Manufacturing of Protein Hydrolysates, Chapter II. In: Protein hydrolysated in Biotechnology, Pasupuleti V.K., Demain A.L. (eds), pp. 11–32.10.1007/978-1-4020-6674-0_2Search in Google Scholar

Penn M.H., Bendiksen E.A., Campbell P., Krogdahl A. (2011). High level of dietary pea protein concentrate induces enteropathy in Atlantic salmon (Salmo salar L.). Aquaculture, 310: 267–273.10.1016/j.aquaculture.2010.10.040Search in Google Scholar

Piccolo G., Iaconisi V., Marono S., Gasco L., Loponte R.Nizza S., Bovera F. (2017). Effect of Tenebrio molitor larvae meal on growth performance, in vivo nutrients digestibility, somatic and marketable indexes of gilthead sea bream (Sparus aurata). Anim. Feed Sci. Technol., 226: 12–20.10.1016/j.anifeedsci.2017.02.007Search in Google Scholar

Refstie S., Olli J.J., Standald H. (2004). Feed intake, growth, and protein utilisation by post-smolt Atlantic salmon (Salmo salar) in response to graded levels of fish protein hydrolysate in the diet. Aquaculture, 239: 331–349.10.1016/j.aquaculture.2004.06.015Search in Google Scholar

Refstie S., Bakke A.M., Petcare M., Penn M.H., Sundby A., Shearer K., Krog-dahl A. (2006 a). Capacity for digestive hydrolysis and amino acid absorption in Atlantic salmon (Salmo salar) fed diets with soybean meal or inulin or without addition of antibiotics. Aquaculture, 261: 392–406.10.1016/j.aquaculture.2006.08.005Search in Google Scholar

Refstie S., Glencross B., Landsverk T., Sørensen M., Lilleeng E., Hawkins W., Krogdahl A. (2006 b). Digestive function and intestinal integrity in Atlantic salmon (Salmo salar) fed kernel meals and protein concentrates made from yellow or narrow-leafed lupins. Aqua-culture, 261: 1382–1395.10.1016/j.aquaculture.2006.07.046Search in Google Scholar

Roncarati A., Gasco L., Parisi G., Terova G.. (2015). Growth performance of common catfish (Ameiurus melas Raf.) fingerlings fed mealworm (Tenebrio molitor) diet. J. Insects as Food Feed, 1: 233–240.10.3920/JIFF2014.0006Search in Google Scholar

Rumpold B.A., Klocke M., Schlüter O. (2017). Insect biodiversity: underutilized bioresource for sustainable applications in life sciences. Reg. Environ. Change, 17: 1445–1454.10.1007/s10113-016-0967-6Search in Google Scholar

Sajjadi M., Carter C.G. (2004). Effect of phytic acid and phytase on feed intake, growth, digestibility and trypsin activity in Atlantic salmon (Salmo salar, L.). Aquacult. Nutr., 10: 135–142.10.1111/j.1365-2095.2003.00290.xSearch in Google Scholar

Salze G.P., Davis D.A. (2015). Taurine: a critical nutrient for future fish feeds. Aquaculture, 437: 215–22910.1016/j.aquaculture.2014.12.006Search in Google Scholar

Sandnes K., Lie Ø., Waagbø R. (1988). Normal ranges of some blood chemistry parameters in adult farmed Atlantic salmon, Salmo salar. J. Fish Biol., 32: 129–136.10.1111/j.1095-8649.1988.tb05341.xSearch in Google Scholar

Santigosa E., Sánchez J., Médale F., Kaushik S., Pérez-Sánchez J., Gallar-do M.A. (2008). Modifications of digestive enzymes in trout (Oncorhynchus mykiss) and sea bream (Sparus aurata) in response to dietary fish meal replacement by plant protein sources. Aqua-culture, 282: 68–74.10.1016/j.aquaculture.2008.06.007Search in Google Scholar

Sánchez-Muros M., García-Rejón L., García-Salguero L., dela Higuera M., Lupiáñez J.A. (1998). Long-term nutritional effects on the primary liver and kidney metabolism in rainbow trout. Adaptive response to starvation and a high-protein, carbohydrate-free diet on glutamate dehydrogenase and alanine aminotransferase kinetics. Int. J. Biochem. Cell Biol., 30: 55–63.10.1016/S1357-2725(97)00100-3Search in Google Scholar

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: 16–27.10.1016/j.jclepro.2013.11.068Search in Google Scholar

Sánchez-Muros M.J., De Haro C., Sanz A., Trenzado C.E., Villareces S., Bar-roso F.G. (2016). Nutritional evaluation of Tenebrio molitor meal as fishmeal substitute for tilapia (Oreochromis niloticus) diet. Aquacult. Nutr., 22: 943–955.10.1111/anu.12313Search in Google Scholar

Stamer A. (2015). Insect proteins a new source for animal feed. Sci. Soc., 16: 676–680.10.15252/embr.201540528Search in Google Scholar

Storebakken T. (2002). Atlantic salmon, Salmo salar. In: Nutrient Requirements and Feeding of Finfish for Aquaculture, Webster C. (ed.). Aquaculture Research Center, Kentucky State University, USA, Chhorn Lim, USDA-ARS, Fish Diseases and Parasites Research Laboratory, Auburn, Alabama, USA.Search in Google Scholar

Su J., Gong Y., Cao S., Lu F., Han D., Liu H., Jin J., Yang X., 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 Immun., 69: 59–66.10.1016/j.fsi.2017.08.008Search in Google Scholar

Torrissen K.R., Lied E., Espe M. (1994). Differences in digestion and absorption of dietary protein in Atlantic salmon (Salmo salar) with genetically different trypsin isozymes. J. Fish Biol., 45: 1087–1104.10.1111/j.1095-8649.1994.tb01075.xSearch in Google Scholar

Van Huis A., Van Itterbeeck J., Klunder H., Mertens E., Halloran A., Muir G., Vantomme P. (2013). Edible insects: future prospects for food and feed security. Food and Agriculture Organization of the United Nations. Forestry Paper No. 171. Rome, 2013.Search in Google Scholar

Vercruysse L., Smagghe G., Beckers T., Van Camp J. (2009). Antioxidative and ACE inhibitory activities in enzymatic hydrolysates of the cotton leafworm, Spodoptera littoralis. Food Chem., 114: 38–43.10.1016/j.foodchem.2008.09.011Search in Google Scholar

Wang Y., Dang X., Zheng X., Zhang W. (2013). Housefly larvae hydrolysate: orthogonal optimization of hydrolysis, antioxidant activity, amino acid composition and functional properties. BMC Research Notes, 6: 197.10.1186/1756-0500-6-197Search in Google Scholar

Was A., Wenne R. (2002). Genetic differentiation in hatchery and wild sea trout (Salmo trutta) in the Southern Baltic at microsatellite loci. Aquaculture, 204: 493–506.10.1016/S0044-8486(01)00835-3Search in Google Scholar

Witkowski A., Kotusz J., Przybylski M. (2009). The degree of threat to the freshwater ichthyofauna of Poland: Red list of fishes and lampreys – situation in 2009 (in Polish). Chrońmy Przyrodę Ojczystą, 65: 33–52.Search in Google Scholar

Zheng K., Liang M., Yao H., Wang J., Chang Q. (2012). Effect of dietary fish protein hydro-lysate on growth, feed utilization and IGF-1 levels in Japanese flounder (Paralichthys olivaceus). Aquacult. Nutr., 18: 297–303.10.1111/j.1365-2095.2011.00896.xSearch in Google Scholar