Spirulina-enriched Substrate to Rear Black Soldier Fly (Hermetia illucens) Prepupae as Alternative Aquafeed Ingredient for Rainbow Trout (Oncorhynchus mykiss) Diets: Possible Effects on Zootechnical Performances, Gut and Liver Health Status, and Fillet Quality

Simple Summary To promote sustainability in aquaculture, the black soldier fly deserves special attention as an alternative ingredient for aquafeed formulation. The present study proposed the inclusion of spirulina in the growth substrate of black soldier fly prepupae to enrich their final biomass in terms of polyunsaturated fatty acids and antioxidant molecules. The obtained prepupae meal was used as a replacer of unsustainable marine-derived ingredients in diets intended for rainbow trout during a 6-week feeding trial. The results showed that fish zootechnical performances, gut and liver health status, and marketable characteristics were not negatively affected by the experimental diets. Abstract In the present study, an organic substrate (coffee silverskin) enriched with spirulina (Arthrospira platensis; 15% w/w), as a source of lipids and bioactive molecules, was used to rear the black soldier fly (Hermetia illucens) prepupae. Three grossly isonitrogenous, isoproteic, isolipidic and isoenergetic experimental diets for rainbow trout (Oncorhynchus mykiss) juveniles were then produced: a control diet (HM0) mostly including fish meal and fish oil, and two other test diets named HM3 and HM20, in which 3 or 20% of the marine ingredients were substituted with full fat black soldier fly prepupae meal (HM), respectively. Experimental diets were provided for 6 weeks, and at the end of the trial the physiological responses and marketable traits of the fish were investigated using a multidisciplinary approach. Generally, all test diets were well accepted, and fish growth, gut and liver health status, and marketable characteristics were not impaired by the experimental diets. However, an increased immuno-related gene expression along with a slight reduction of fillet redness and yellowness was evident in fish from the HM20 group.

[1]  N. Revathi,et al.  Use of black soldier fly (Hermetia illucens L.) larvae meal in aquafeeds for a sustainable aquaculture industry: A review of past and future needs , 2022, Aquaculture.

[2]  E. Giorgini,et al.  Conventional feed additives or red claw crayfish meal and dried microbial biomass as feed supplement in fish meal-free diets for rainbow trout (Oncorhynchus mykiss): Possible ameliorative effects on growth and gut health status , 2022, Aquaculture.

[3]  P. Riolo,et al.  Effects of black soldier fly (Hermetia illucens) enriched with Schizochytrium sp. on zebrafish (Danio rerio) reproductive performances , 2021, Aquaculture.

[4]  J. Tetens,et al.  Total Replacement of Fishmeal by Spirulina (Arthrospira platensis) and Its Effect on Growth Performance and Product Quality of African Catfish (Clarias gariepinus) , 2021, Sustainability.

[5]  G. C. Zittelli,et al.  Chemical composition and apparent digestibility of a panel of dried microalgae and cyanobacteria biomasses in rainbow trout (Oncorhynchus mykiss) , 2021 .

[6]  K. El-Tarabily,et al.  Nutritional applications of species of Spirulina and Chlorella in farmed fish: A review , 2021 .

[7]  E. Giorgini,et al.  Application of laboratory methods for understanding fish responses to black soldier fly (Hermetia illucens) based diets , 2021 .

[8]  Shivatharsiny Yohi,et al.  Potential natural carotenoid sources for the colouration of ornamental fish: a review , 2021, Aquaculture International.

[9]  P. Riolo,et al.  Possible Dietary Effects of Insect-Based Diets across Zebrafish (Danio rerio) Generations: A Multidisciplinary Study on the Larval Phase , 2021, Animals : an open access journal from MDPI.

[10]  E. Giorgini,et al.  Hermetia illucens and Poultry by-Product Meals as Alternatives to Plant Protein Sources in Gilthead Seabream (Sparus aurata) Diet: A Multidisciplinary Study on Fish Gut Status , 2021, Animals : an open access journal from MDPI.

[11]  E. Giorgini,et al.  Physiological response of rainbow trout (Oncorhynchus mykiss) to graded levels of Hermetia illucens or poultry by-product meals as single or combined substitute ingredients to dietary plant proteins , 2021 .

[12]  P. Falcone,et al.  Impact of Mild Oven Cooking Treatments on Carotenoids and Tocopherols of Cheddar and Depurple Cauliflower (Brassica oleracea L. var. botrytis) , 2021, Antioxidants.

[13]  V. Milanović,et al.  Physiological responses of Siberian sturgeon (Acipenser baerii) juveniles fed on full-fat insect-based diet in an aquaponic system , 2021, Scientific reports.

[14]  L. Aquilanti,et al.  Microbial dynamics in rearing trials of Hermetia illucens larvae fed coffee silverskin and microalgae. , 2020, Food research international.

[15]  L. Bruni,et al.  Dietary inclusion of full-fat Hermetia illucens prepupae meal in practical diets for rainbow trout (Oncorhynchus mykiss): Lipid metabolism and fillet quality investigations , 2020 .

[16]  F. G. Barroso,et al.  Potential use of black soldier fly ( Hermetia illucens ) and mealworm ( Tenebrio molitor ) insectmeals in diets for rainbow trout ( Oncorhynchus mykiss ) , 2020 .

[17]  Luca Tiano,et al.  Impact of traditional and mild oven cooking treatments on antioxidant compounds levels and oxidative status of Atlantic salmon (Salmo salar) fillets , 2020 .

[18]  Sehrish Taj,et al.  Effects of replacement of fish meal by poultry by-product meal on growth performance and gene expression involved in protein metabolism for juvenile black sea bream (Acanthoparus schlegelii) , 2020 .

[19]  T. Nakano,et al.  Properties of Carotenoids in Fish Fitness: A Review , 2020, Marine drugs.

[20]  Christopher M. Free,et al.  The future of food from the sea , 2020, Nature.

[21]  D. Józefiak,et al.  The Effect of Hydrolyzed Insect Meals in Sea Trout Fingerling (Salmo trutta m. trutta) Diets on Growth Performance, Microbiota and Biochemical Blood Parameters , 2020, Animals : an open access journal from MDPI.

[22]  Vikas Kumar,et al.  A review on Spirulina: alternative media for cultivation and nutritive value as an aquafeed , 2020, Reviews in Aquaculture.

[23]  S. Mousavi,et al.  A review on insect meals in aquaculture: the immunomodulatory and physiological effects , 2020 .

[24]  B. Halpern,et al.  Global adoption of novel aquaculture feeds could substantially reduce forage fish demand by 2030 , 2020, Nature Food.

[25]  F. Zhang,et al.  Application of Spirulina in aquaculture: a review on wastewater treatment and fish growth , 2020, Reviews in Aquaculture.

[26]  Yanxian Li,et al.  Total replacement of fish meal with black soldier fly (Hermetia illucens) larvae meal does not compromise the gut health of Atlantic salmon (Salmo salar) , 2020 .

[27]  R. Pasquariello,et al.  A Detailed Study of Rainbow Trout (Onchorhynchus mykiss) Intestine Revealed That Digestive and Absorptive Functions Are Not Linearly Distributed along Its Length , 2020, Animals : an open access journal from MDPI.

[28]  V. Milanović,et al.  Black Soldier Fly (Hermetia illucens) reared on roasted coffee by-product and Schizochytrium sp. as a sustainable terrestrial ingredient for aquafeeds production , 2020 .

[29]  C. Lalander,et al.  Fatty acid composition of black soldier fly larvae (Hermetia illucens) - Possibilities and limitations for modification through diet. , 2020, Waste management.

[30]  C. Conti,et al.  Investigation of human pancreatic cancer tissues by Fourier Transform Infrared Hyperspectral Imaging , 2019, Journal of biophotonics.

[31]  Dong Han,et al.  Effects of dietary Arthrospira platensis supplementation on the growth, pigmentation, and antioxidation in yellow catfish (Pelteobagrus fulvidraco) , 2019, Aquaculture.

[32]  B. Costas,et al.  The Use of Dietary Additives in Fish Stress Mitigation: Comparative Endocrine and Physiological Responses , 2019, Front. Endocrinol..

[33]  A. Józefiak,et al.  The Utilization of Full-Fat Insect Meal in Rainbow Trout (Oncorhynchus mykiss) Nutrition: The Effects on Growth Performance, Intestinal Microbiota and Gastrointestinal Tract Histomorphology , 2019, Annals of Animal Science.

[34]  E. Giorgini,et al.  A six-months study on Black Soldier Fly (Hermetia illucens) based diets in zebrafish , 2019, Scientific Reports.

[35]  N. Sheikhzadeh,et al.  Spirulina platensis in rainbow trout (Oncorhynchus mykiss) feed: effects on growth, fillet composition, and tissue antioxidant mechanisms , 2019, Aquaculture International.

[36]  Wenguang Zhou,et al.  A Review on the Use of Microalgae for Sustainable Aquaculture , 2019, Applied Sciences.

[37]  R. Nielsen,et al.  Aquaculture subsidies in the European Union: Evolution, impact and future potential for growth , 2019, Marine Policy.

[38]  L. Bruni,et al.  Effects of Graded Dietary Inclusion Level of Full-Fat Hermetia illucens Prepupae Meal in Practical Diets for Rainbow Trout (Oncorhynchus mykiss) , 2019, Animals : an open access journal from MDPI.

[39]  A. Mathys,et al.  Sustainable use of Hermetia illucens insect biomass for feed and food: Attributional and consequential life cycle assessment , 2019, Resources, Conservation and Recycling.

[40]  H. Byrne,et al.  Vibrational characterization of granulosa cells from patients affected by unilateral ovarian endometriosis: New insights from infrared and Raman microspectroscopy. , 2019, Spectrochimica acta. Part A, Molecular and biomolecular spectroscopy.

[41]  Yanxian Li,et al.  Black soldier fly larvae meal can replace fish meal in diets of sea-water phase Atlantic salmon (Salmo salar) , 2019, Aquaculture.

[42]  Å. Berggren,et al.  Approaching Ecological Sustainability in the Emerging Insects-as-Food Industry. , 2019, Trends in ecology & evolution.

[43]  E. Tibaldi,et al.  Intestinal morpho-physiology and innate immune status of European sea bass (Dicentrarchus labrax) in response to diets including a blend of two marine microalgae, Tisochrysis lutea and Tetraselmis suecica , 2019, Aquaculture.

[44]  M. Najafi,et al.  The effect of Spirulina platensis meal on antioxidant gene expression, total antioxidant capacity, and lipid peroxidation of rainbow trout (Oncorhynchus mykiss) , 2019, Fish Physiology and Biochemistry.

[45]  E. Giorgini,et al.  New insights on the macromolecular building of rainbow trout (O. mykiss) intestine: FTIR Imaging and histological correlative study , 2018, Aquaculture.

[46]  E. Lock,et al.  Insect-based diets high in lauric acid reduce liver lipids in freshwater Atlantic salmon , 2018, Aquaculture Nutrition.

[47]  M. Capucchio,et al.  Influence of Hermetia illucens meal dietary inclusion on the histological traits, gut mucin composition and the oxidative stress biomarkers in rainbow trout (Oncorhynchus mykiss) , 2018, Aquaculture.

[48]  L. Romano,et al.  Feasibility of the use of Spirulina in aquaculture diets , 2018, Reviews in Aquaculture.

[49]  T. Hahn,et al.  New methods for high-accuracy insect chitin measurement. , 2018, Journal of the science of food and agriculture.

[50]  L. Bruni,et al.  Partial Dietary Inclusion of Hermetia illucens (Black Soldier Fly) Full-Fat Prepupae in Zebrafish Feed: Biometric, Histological, Biochemical, and Molecular Implications. , 2018, Zebrafish.

[51]  A. Ferrari,et al.  USING BLACK SOLDIER FLIES (HERMETIA ILLUCENS) TO BIOCONVERT WASTE FROM THE LIVESTOCK PRODUCTION CHAIN: A LIFE CYCLE ASSESSMENT CASE STUDY , 2018, Waste Management and the Environment IX.

[52]  Marcel Dicke,et al.  Influence of larval density and dietary nutrient concentration on performance, body protein, and fat contents of black soldier fly larvae (Hermetia illucens) , 2018, Entomologia experimentalis et applicata.

[53]  E. Giorgini,et al.  Rearing Zebrafish on Black Soldier Fly (Hermetia illucens): Biometric, Histological, Spectroscopic, Biochemical, and Molecular Implications. , 2018, Zebrafish.

[54]  P. Sarker,et al.  Towards sustainable aquafeeds: Evaluating substitution of fishmeal with lipid-extracted microalgal co-product (Nannochloropsis oculata) in diets of juvenile Nile tilapia (Oreochromis niloticus) , 2018, PloS one.

[55]  F. Gai,et al.  Effect of rearing substrate on growth performance, waste reduction efficiency and chemical composition of black soldier fly (Hermetia illucens) larvae. , 2018, Journal of the science of food and agriculture.

[56]  F. G. Barroso,et al.  Insects as Food: Fatty Acid Profiles, Lipid Classes, and sn‐2 Fatty Acid Distribution of Lepidoptera Larvae , 2018 .

[57]  X. Chai,et al.  Replacing fish meal with a blend of poultry by-product meal and feather meal in diets for giant croaker (Nibea japonica). , 2018 .

[58]  S. Chatzifotis,et al.  Does dietary insect meal affect the fish immune system? The case of mealworm, Tenebrio molitor on European sea bass, Dicentrarchus labrax , 2018, Developmental and comparative immunology.

[59]  A. Huis,et al.  Can diets containing insects promote animal health , 2018 .

[60]  E. Giorgini,et al.  The influence of diet on the early development of two seahorse species (H. guttulatus and H. reidi): Traditional and innovative approaches , 2018 .

[61]  Dong Han,et al.  Effects of dietary fishmeal replacement with Spirulina platensis on the growth, feed utilization, digestion and physiological parameters in juvenile gibel carp (Carassis auratus gibelio var. CAS III) , 2018 .

[62]  A. Marseglia,et al.  Composition of black soldier fly prepupae and systematic approaches for extraction and fractionation of proteins, lipids and chitin. , 2018, Food research international.

[63]  G. Parisi,et al.  Mealworm as dietary protein source for rainbow trout: Body and fillet quality traits , 2018 .

[64]  Giovanni Antonio Lutzu,et al.  Microalgae in aquafeeds for a sustainable aquaculture industry , 2018, Journal of Applied Phycology.

[65]  K. Sudhakar,et al.  Spirulina - From growth to nutritional product: A review , 2017 .

[66]  F. G. Barroso,et al.  Insects as food: Enrichment of larvae of Hermetia illucens with omega 3 fatty acids by means of dietary modifications , 2017 .

[67]  E. Lock,et al.  Modulation of nutrient composition of black soldier fly (Hermetia illucens) larvae by feeding seaweed-enriched media , 2017, PloS one.

[68]  C. Dinnella,et al.  Inclusion of Hermetia illucens larvae meal on rainbow trout (Oncorhynchus mykiss) feed: effect on sensory profile according to static and dynamic evaluations. , 2017, Journal of the science of food and agriculture.

[69]  H. Gutzeit,et al.  The black soldier fly, Hermetia illucens – a promising source for sustainable production of proteins, lipids and bioactive substances , 2017, Zeitschrift fur Naturforschung. C, Journal of biosciences.

[70]  H. Peres,et al.  Black soldier fly (Hermetia illucens) pre-pupae meal as a fish meal replacement in diets for European seabass (Dicentrarchus labrax) , 2017 .

[71]  M. Capucchio,et al.  Evaluation of the suitability of a partially defatted black soldier fly (Hermetia illucens L.) larvae meal as ingredient for rainbow trout (Oncorhynchus mykiss Walbaum) diets , 2017, Journal of Animal Science and Biotechnology.

[72]  M. Eeckhout,et al.  Nutritional composition of black soldier fly (Hermetia illucens) prepupae reared on different organic waste substrates. , 2017, Journal of the science of food and agriculture.

[73]  P. Lucci,et al.  Bioactive fatty acids in mantis shrimp, crab and caramote prawn: Their content and distribution among the main lipid classes , 2017 .

[74]  J. Tomberlin,et al.  The Impact of Diet Protein and Carbohydrate on Select Life-History Traits of The Black Soldier Fly Hermetia illucens (L.) (Diptera: Stratiomyidae) , 2017, Insects.

[75]  O. Carnevali,et al.  Growth and stress factors in ballan wrasse (Labrus bergylta) larval development , 2017 .

[76]  Kamarudin,et al.  Growth performance, feed Utilization and body composition of nile tilapia, Oreochromis niloticus (Linnaeus, 1758) fed with different levels of black soldier fly, Hermetia illucens (Linnaeus, 1758) maggot meal diet , 2017 .

[77]  V. Fogliano,et al.  Nitrogen-to-Protein Conversion Factors for Three Edible Insects: Tenebrio molitor, Alphitobius diaperinus, and Hermetia illucens , 2017, Journal of agricultural and food chemistry.

[78]  S. Rawles,et al.  Bio‐Ag reutilization of distiller's dried grains with solubles (DDGS) as a substrate for black soldier fly larvae, Hermetia illucens, along with poultry by‐product meal and soybean meal, as total replacement of fish meal in diets for Nile tilapia, Oreochromis niloticus , 2016 .

[79]  Robert Manurung,et al.  Bioconversion of Rice straw waste by black soldier fly larvae (Hermetia illucens L.) : Optimal feed rate for biomass production , 2016 .

[80]  D. Tocher Omega-3 long-chain polyunsaturated fatty acids and aquaculture in perspective , 2015 .

[81]  Vito Librando,et al.  Vibrational mapping of sinonasal lesions by Fourier transform infrared imaging spectroscopy , 2015, Journal of biomedical optics.

[82]  G. Mosconi,et al.  The effects of starving and feeding on Dover sole (Solea solea, Soleidae, Linnaeus, 1758) stress response and early larval development , 2015 .

[83]  G. Saccone,et al.  Omega-3 long-chain polyunsaturated fatty acids and fish oil supplementation during pregnancy: which evidence? , 2015, The journal of maternal-fetal & neonatal medicine : the official journal of the European Association of Perinatal Medicine, the Federation of Asia and Oceania Perinatal Societies, the International Society of Perinatal Obstetricians.

[84]  Merab A. Chan,et al.  Dietary Spirulina (Arthrospira platensis) replacement enhances performance of juvenile Nile tilapia (Oreochromis niloticus) , 2015, Journal of Applied Phycology.

[85]  R. Pal,et al.  Microalgae in Aquaculture: A Review with Special References to Nutritional Value and Fish Dietetics , 2015, Proceedings of the Zoological Society.

[86]  J. Dalsgaard,et al.  Dietary methionine level affects growth performance and hepatic gene expression of GH-IGF system and protein turnover regulators in rainbow trout (Oncorhynchus mykiss) fed plant protein-based diets. , 2015, Comparative biochemistry and physiology. Part B, Biochemistry & molecular biology.

[87]  M. Bonini,et al.  Transfer of silica-coated magnetic (Fe3O4) nanoparticles through food: a molecular and morphological study in zebrafish. , 2014, Zebrafish.

[88]  Gilles Tran,et al.  State-of-the-art on use of insects as animal feed. , 2014 .

[89]  O. Carnevali,et al.  Probiotic Supplementation Promotes Calcification in Danio rerio Larvae: A Molecular Study , 2013, PloS one.

[90]  M. Borkovcová,et al.  The effect of dietary Salvia hispanica seed on the content of n-3 long-chain polyunsaturated fatty acids in tissues of selected animal species, including edible insects , 2013 .

[91]  J. Tomberlin,et al.  Influence of Resources on Hermetia illucens. (Diptera: Stratiomyidae) Larval Development , 2013, Journal of medical entomology.

[92]  M. Teimouri,et al.  The effects of Spirulina platensis meal as a feed supplement on growth performance and pigmentation of rainbow trout (Oncorhynchus mykiss) , 2013 .

[93]  K. Dąbrowski,et al.  Enhancing the growth of Nile tilapia larvae/juveniles by replacing plant (gluten) protein with algae protein , 2013 .

[94]  Robert S. Leiken A User’s Guide , 2011 .

[95]  Malcolm Jobling,et al.  National Research Council (NRC): Nutrient requirements of fish and shrimp , 2011, Aquaculture International.

[96]  O. Carnevali,et al.  Live prey enrichment, with particular emphasis on HUFAs, as limiting factor in false percula clownfish (Amphiprion ocellaris, Pomacentridae) larval development and metamorphosis: molecular and biochemical implications. , 2011, Comparative biochemistry and physiology. Part A, Molecular & integrative physiology.

[97]  J. Tomberlin,et al.  Sensory Analysis of Rainbow Trout, Oncorhynchus mykiss, Fed Enriched Black Soldier Fly Prepupae, Hermetia illucens , 2011 .

[98]  J. Verreth,et al.  Time-related changes of the intestinal morphology of Atlantic salmon, Salmo salar L., at two different soybean meal inclusion levels. , 2009, Journal of fish diseases.

[99]  S. Diener,et al.  Conversion of organic material by black soldier fly larvae: establishing optimal feeding rates , 2009, Waste management & research : the journal of the International Solid Wastes and Public Cleansing Association, ISWA.

[100]  G. Turchini,et al.  Fish oil replacement in finfish nutrition , 2009 .

[101]  J. Elias,et al.  Chitin regulation of immune responses: an old molecule with new roles. , 2008, Current opinion in immunology.

[102]  Wei Liu,et al.  TLR-2 and IL-17A in Chitin-Induced Macrophage Activation and Acute Inflammation1 , 2008, The Journal of Immunology.

[103]  S. Paik,et al.  Crystal Structure of the TLR1-TLR2 Heterodimer Induced by Binding of a Tri-Acylated Lipopeptide , 2007, Cell.

[104]  J. Milner,et al.  A review of the interaction among dietary antioxidants and reactive oxygen species. , 2007, The Journal of nutritional biochemistry.

[105]  J. G. Bell,et al.  Does dietary tocopherol level affect fatty acid metabolism in fish? , 2007, Fish Physiology and Biochemistry.

[106]  J. M. Gallardo,et al.  Comparison of six methylation methods for analysis of the fatty acid composition of albacore lipid , 2007 .

[107]  K. Dąbrowski,et al.  Expanding the utilization of sustainable plant products in aquafeeds: a review , 2007 .

[108]  M. Cardinali,et al.  Diplodus sargus interrenal-pituitary response: chemical communication in stressed fish. , 2002, General and comparative endocrinology.

[109]  J. Tomberlin,et al.  Selected Life-History Traits of Black Soldier Flies (Diptera: Stratiomyidae) Reared on Three Artificial Diets , 2002 .

[110]  W. Christie A simple procedure for rapid transmethylation of glycerolipids and cholesteryl esters. , 1982, Journal of lipid research.

[111]  J. Folch,et al.  A simple method for the isolation and purification of total lipides from animal tissues. , 1957, The Journal of biological chemistry.

[112]  C. Conti,et al.  Fatty acids profile of black soldier fly (Hermetia illucens): Influence of feeding substrate based on coffee-waste silverskin enriched with microalgae , 2020 .

[113]  D. Kamilya,et al.  Chitin and chitosan as promising immunostimulant for aquaculture , 2020 .

[114]  A. Krüger-Genge,et al.  Spirulina platensis, a super food? , 2019, Journal of Cellular Biotechnology.

[115]  E. Giorgini,et al.  Insect meal based diets for clownfish: Biometric, histological, spectroscopic, biochemical and molecular implications , 2019, Aquaculture.

[116]  Sebastian S. Mosha The Significance of Spirulina Meal on Fishmeal Replacement in Aquaculture. A Review , 2019 .

[117]  Ó. Monroig,et al.  Polyunsaturated Fatty Acid Biosynthesis and Metabolism in Fish , 2018 .

[118]  I. Priyadarshani,et al.  Commercial and industrial applications of micro algae - A review , 2012 .

[119]  J. Dick,et al.  Pyloric ceca are significant sites of newly synthesized 22∶6n−3 in rainbow trout (Oncorhynchus mykiss) , 2003, Lipids.

[120]  E. P. Lewis In perspective. , 1972, Nursing outlook.