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

Simple Summary Sustainability and fish welfare have been receiving increasing attention in the aquaculture sector, with an emphasis on the search for new, sustainable, and healthy aquafeed ingredients. For many years, plant ingredients have been widely used in aquafeed formulation; however, negative side effects on gut welfare have often been reported in several carnivorous fish species. From this perspective, alternative ingredients such as poultry by-products and insect meal are receiving attention due to their low ecological footprint and high nutritional value. In the present study, these two ingredients were used, singly or in combination, to formulate practical diets for gilthead seabream (Sparus aurata). After a twelve-week feeding trial, a multidisciplinary laboratory approach including histological, molecular, and spectroscopic techniques was adopted in order to investigate fish physiological responses to the new test diets. The results obtained showed excellent zootechnical performances and ameliorated gut health in fish fed dietary inclusions of poultry by-products and insect meal compared to those fed a vegetable-based diet. In addition, the modulation of nutrient absorption in relation to the ingredients used was highlighted by means of spectroscopic tools. The results obtained demonstrated that poultry by-products and insect meal can be successfully used to replace plant-derived ingredients in diets for gilthead seabream without negatively affecting fish welfare. Abstract The attempt to replace marine-derived ingredients for aquafeed formulation with plant-derived ones has met some limitations due to their negative side effects on many fish species. In this context, finding new, sustainable ingredients able to promote fish welfare is currently under exploration. In the present study, poultry by-products and Hermetia illucens meal were used to replace the vegetable protein fraction in diets totally deprived of fish meal intended for gilthead seabream (Sparus aurata). After a 12-week feeding trial, a multidisciplinary approach including histological, molecular, and spectroscopic techniques was adopted to investigate intestine and liver responses to the different dietary formulations. Regardless of the alternative ingredient used, the reduction in dietary vegetable proteins resulted in a lower incidence of intestine histological alterations and inflammatory responses. In addition, the dietary inclusion of insect meal positively affected the reduction in the molecular inflammatory markers analyzed. Spectroscopic analyses showed that poultry by-product meal improved lipid absorption in the intestine, while insect meal induced increased liver lipid deposition in fish. The results obtained demonstrated that both poultry by-products and H. illucens meal can successfully be used to replace plant-derived ingredients in diets for gilthead seabream, promoting healthy aquaculture.

[1]  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.

[2]  L. Gasco,et al.  Beyond the protein concept: health aspects of using edible insects on animals , 2020, Journal of Insects as Food and Feed.

[3]  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 .

[4]  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 .

[5]  Vikas Kumar,et al.  The Potential Impacts of Soy Protein on Fish Gut Health , 2020, Soybean for Human Consumption and Animal Feed.

[6]  O. Carnevali,et al.  Can Insect-Based Diets Affect Zebrafish (Danio rerio) Reproduction? A Multidisciplinary Study. , 2020, Zebrafish.

[7]  Abdelrazeq M. Shehata,et al.  Black Soldier Fly (Hermetia illucens) Meal as a Promising Feed Ingredient for Poultry: A Comprehensive Review , 2020, Agriculture.

[8]  V. Milanović,et al.  Zebrafish (Danio rerio) physiological and behavioural responses to insect-based diets: a multidisciplinary approach , 2020, Scientific Reports.

[9]  I. García-Meilán,et al.  Effects of different dietary vegetable oils on growth and intestinal performance, lipid metabolism and flesh quality in gilthead sea bream , 2020 .

[10]  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 .

[11]  W. Yao,et al.  Effects of replacing fishmeal protein with poultry by-product meal protein and soybean meal protein on growth, feed intake, feed utilization, gut and liver histology of hybrid grouper (Epinephelus fuscoguttatus ♀ × Epinephelus lanceolatus ♂) juveniles , 2020 .

[12]  S. Chatzifotis,et al.  Honey Bee Pollen in Meagre (Argyrosomus regius) Juvenile Diets: Effects on Growth, Diet Digestibility, Intestinal Traits, and Biochemical Markers Related to Health and Stress , 2020, Animals : an open access journal from MDPI.

[13]  H. Abdel‐Ghany,et al.  Effects of dietary chitosan supplementation on farmed fish; a review , 2020, Reviews in Aquaculture.

[14]  L. Aquilanti,et al.  Hermetia illucens in diets for zebrafish (Danio rerio): A study of bacterial diversity by using PCR-DGGE and metagenomic sequencing , 2019, PloS one.

[15]  Alan E. Wilson,et al.  Success of fishmeal replacement through poultry by‐product meal in aquaculture feed formulations: a meta‐analysis , 2019 .

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

[17]  C. Feijóo,et al.  Anti-inflammatory effects of aloe vera on soy meal-induced intestinal inflammation in zebrafish. , 2019, Fish & shellfish immunology.

[18]  R. Schiavone,et al.  Poultry by-product meal as an alternative to fish meal in the juvenile gilthead seabream (Sparus aurata) diet , 2019, Aquaculture.

[19]  W. Gallardo,et al.  Attractability and palatability of formulated diets incorporated with chicken feather and algal meals for juvenile gilthead seabream, Sparus aurata , 2019, Aquaculture Reports.

[20]  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.

[21]  B. Neto,et al.  Life cycle assessment of diets for gilthead seabream (Sparus aurata) with different protein/carbohydrate ratios and fishmeal or plant feedstuffs as main protein sources , 2019, The International Journal of Life Cycle Assessment.

[22]  H. M. Munang'andu,et al.  Gut health and vaccination response in pre‐smolt Atlantic salmon (Salmo salar) fed black soldier fly (Hermetia illucens) larvae meal , 2019, Fish & shellfish immunology.

[23]  H. Peres,et al.  Soybean meal replacement by corn distillers dried grains with solubles (DDGS) and exogenous non-starch polysaccharidases supplementation in diets for gilthead seabream (Sparus aurata) juveniles , 2019, Aquaculture.

[24]  G. Berben,et al.  Survey of animal by-products in feedingstuffs before the reintroduction of processed animal proteins in aquafeed , 2019, BASE.

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

[26]  A. Cellerino,et al.  Breeders Age Affects Reproductive Success in Nothobranchius furzeri. , 2018, Zebrafish.

[27]  M. Collado,et al.  Long-term feeding with high plant protein based diets in gilthead seabream (Sparus aurata, L.) leads to changes in the inflammatory and immune related gene expression at intestinal level , 2018, BMC Veterinary Research.

[28]  P. Gobbi,et al.  Insect meals in fish nutrition , 2018, Reviews in Aquaculture.

[29]  E. Mente,et al.  Effect of fishmeal replacement by poultry by-product meal on growth performance, proximate composition, digestive enzyme activity, haematological parameters and gene expression of gilthead seabream (Sparus aurata ) , 2018, Aquaculture Nutrition.

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

[31]  T. Hanson,et al.  Effects of soybean meal replacement with fermented soybean meal on growth, serum biochemistry and morphological condition of liver and distal intestine of Florida pompano Trachinotus carolinus , 2018 .

[32]  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 .

[33]  E. Skřivanová,et al.  Susceptibility of Escherichia coli, Salmonella sp and Clostridium perfringens to organic acids and monolaurin , 2018 .

[34]  Zhigang Zhou,et al.  Dietary effects of soybean products on gut microbiota and immunity of aquatic animals: A review , 2018 .

[35]  K. Mai,et al.  Substituting fish meal with soybean meal in diets for Japanese seabass (Lateolabrax japonicus): Effects on growth, digestive enzymes activity, gut histology, and expression of gut inflammatory and transporter genes , 2018 .

[36]  Gabriella Caruso,et al.  Fishmeal Alternative Protein Sources for Aquaculture Feeds , 2018 .

[37]  M. Eeckhout,et al.  Gut antimicrobial effects and nutritional value of black soldier fly (Hermetia illucens L.) prepupae for weaned piglets , 2018 .

[38]  H. Gutzeit,et al.  Nutritional immunology: Diversification and diet‐dependent expression of antimicrobial peptides in the black soldier fly Hermetia illucens , 2018, Developmental and comparative immunology.

[39]  S. Kaushik,et al.  Disease resistance and response against Vibrio anguillarum intestinal infection in European seabass (Dicentrarchus labrax) fed low fish meal and fish oil diets , 2017, Fish & shellfish immunology.

[40]  E. Sarropoulou,et al.  Effects of graded dietary levels of soy protein concentrate supplemented with methionine and phosphate on the immune and antioxidant responses of gilthead sea bream (Sparus aurata L.) , 2017, Fish & shellfish immunology.

[41]  G. Parisi,et al.  Effect of Tenebrio molitor larvae meal on growth performance, in vivo nutrients digestibility, somatic and marketable indexes of gilthead sea bream (Sparus aurata) , 2017 .

[42]  M. Minghetti,et al.  A fish intestinal epithelial barrier model established from the rainbow trout (Oncorhynchus mykiss) cell line, RTgutGC , 2017, Cell Biology and Toxicology.

[43]  Sara Moutinho,et al.  Meat and bone meal as partial replacement for fish meal in diets for gilthead seabream (Sparus aurata) juveniles: Growth, feed efficiency, amino acid utilization, and economic efficiency , 2017 .

[44]  Yongan Zhang,et al.  Fish gut-liver immunity during homeostasis or inflammation revealed by integrative transcriptome and proteome studies , 2016, Scientific Reports.

[45]  C. Secombes,et al.  The Function of Fish Cytokines , 2016, Biology.

[46]  J. Carral,et al.  Evaluation of poultry by‐product meal as partial replacement of fish meal in practical diets for juvenile tench (Tinca tinca L.) , 2016 .

[47]  S. Martínez‐Llorens,et al.  Potential use of high levels of vegetal proteins in diets for market-sized gilthead sea bream (Sparus aurata) , 2016, Archives of animal nutrition.

[48]  R. Yasothai.  ANTINUTRITIONAL FACTORS IN SOYBEAN MEAL AND ITS DEACTIVATION , 2016 .

[49]  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 .

[50]  G. Piccolo,et al.  Review on the use of insects in the diet of farmed fish: Past and future , 2015 .

[51]  F. G. Barroso,et al.  Insect larvae as feed ingredient selectively increase arachidonic acid content in farmed gilthead sea bream (Sparus aurata L.) , 2015 .

[52]  A. Ray,et al.  The Gastrointestinal Tract of Fish , 2014 .

[53]  B. Yao,et al.  The effect of dietary chitin on the autochthonous gut bacteria of Atlantic cod (Gadus morhua L.) , 2013 .

[54]  B. Koop,et al.  Early response of gene expression in the distal intestine of Atlantic salmon (Salmo salar L.) during the development of soybean meal induced enteritis. , 2013, Fish & shellfish immunology.

[55]  J. Meseguer,et al.  Histological alterations and microbial ecology of the intestine in gilthead seabream (Sparus aurata L.) fed dietary probiotics and microalgae , 2012, Cell and Tissue Research.

[56]  M. Kentouri,et al.  Growth performance, feed utilization and non-specific immune response of gilthead sea bream (Sparus aurata L.) fed graded levels of a bioprocessed soybean meal , 2012 .

[57]  Å. Krogdahl,et al.  Transcriptional regulation of IL-17A and other inflammatory markers during the development of soybean meal-induced enteropathy in the distal intestine of Atlantic salmon (Salmo salar L.). , 2012, Cytokine.

[58]  N. Nogueira,et al.  Inclusion of Low Levels of Blood and Feathermeal in Practical Diets For Gilthead Seabream (Sparus aurata) , 2012 .

[59]  F. Gai,et al.  Enzymatic and Histological Evaluations of Gut and Liver in Rainbow Trout, Oncorhynchus mykiss, Fed with Rice Protein Concentrate-based Diets , 2012 .

[60]  D. Davis,et al.  Replacement of fishmeal with poultry by-product meal in the diet of Florida pompano Trachinotus carolinus L. , 2012 .

[61]  Peng Li,et al.  Evaluation of poultry by-product meal in commercial diets for juvenile cobia (Rachycentron canadum) , 2011 .

[62]  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.

[63]  R. Hardy.  Utilization of plant proteins in fish diets: effects of global demand and supplies of fishmeal , 2010 .

[64]  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.

[65]  Ø. Evensen,et al.  Pro-inflammatory cytokine expression and respiratory burst activity following replacement of fish oil with rapeseed oil in the feed for Atlantic salmon (Salmo salar L.). , 2009 .

[66]  D. Bureau,et al.  Development of a model to estimate digestible lipid content of salmonid fish feeds , 2009 .

[67]  S. Kaushik,et al.  Modifications of digestive enzymes in trout (Oncorhynchus mykiss) and sea bream (Sparus aurata) in response to dietary fish meal replacement by plant protein sources , 2008 .

[68]  P. Gatta,et al.  Influence of dietary levels of soybean meal on the performance and gut histology of gilthead sea bream (Sparus aurata L.) and European sea bass (Dicentrarchus labrax L.) , 2008 .

[69]  L. Mydland,et al.  Lipid digestibility, bile drainage and development of morphological intestinal changes in rainbow trout (Oncorhynchus mykiss) fed diets containing defatted soybean meal , 2008 .

[70]  S. Kaushik,et al.  Effect of high-level fish meal replacement by plant proteins in gilthead sea bream (Sparus aurata) on growth and body/fillet quality traits , 2007 .

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

[72]  S. Martínez‐Llorens,et al.  Soybean meal as a protein source in gilthead sea bream (Sparus aurata L.) diets: effects on growth and nutrient utilization , 2007 .

[73]  M. Marounek,et al.  Susceptibility of Clostridium perfringens to C2–C18 fatty acids , 2005, Letters in applied microbiology.

[74]  Å. Krogdahl,et al.  Carbohydrates in fish nutrition: digestion and absorption in postlarval stages , 2005 .

[75]  K. Mai,et al.  Apparent digestibility of selected feed ingredients for juvenile cobia Rachycentron canadum , 2004 .

[76]  O. Carnevali,et al.  Cloning and expression of high choriolytic enzyme, a component of the hatching enzyme system, during embryonic development of the marine ornamental fish Chrysiptera parasema , 2004 .

[77]  S. Bai,et al.  Effects of dehulled soybean meal as a fish meal replacer in diets for fingerling and growing Korean rockfish Sebastes schlegeli , 2004 .

[78]  Aires Oliva‐Teles.  Recent advances in European sea bass and gilthead sea bream nutrition , 2000, Aquaculture International.

[79]  Å. Krogdahl,et al.  Effects of graded levels of standard soybean meal on intestinal structure, mucosal enzyme activities, and pancreatic response in Atlantic salmon (Salmo salar L.) , 2003 .

[80]  M. Alexis,et al.  Effect of extrusion of wheat and corn on gilthead sea bream (Sparus aurata) growth, nutrient utilization efficiency, rates of gastric evacuation and digestive enzyme activities , 2003 .

[81]  J. Meseguer,et al.  In vitro effect of chitin particles on the innate cellular immune system of gilthead seabream (Sparus aurata L.). , 2003, Fish & shellfish immunology.

[82]  C. Cho,et al.  Apparent digestibility of rendered animal protein ingredients for rainbow trout Oncorhynchus / mykiss , 1999 .

[83]  M. Alexis,et al.  High inclusion levels of poultry meals and related byproducts in diets for gilthead seabream Sparus aurata L. , 1999 .

[84]  A. Oliva‐Teles,et al.  Apparent digestibility coefficients of feedstuffs in seabass (Dicentrarchus labrax) juveniles , 1998 .

[85]  M. Izquierdo,et al.  Corn gluten and meat and bone meals as protein sources in diets for gilthead seabream (Sparus aurata): Nutritional and histological implications , 1997 .

[86]  Guyot,et al.  First events in lipid absorption during post-embryonic development of the anterior intestine in gilt-head sea bream , 1997, Journal of fish biology.

[87]  M. Izquierdo,et al.  Soybean and lupin seed meals as protein sources in diets for gilthead seabream (Sparus aurata): nutritional and histological implications , 1995 .

[88]  Å. Krogdahl,et al.  Soybean trypsin inhibitors in diets for Atlantic salmon (Salmo salar, L): effects on nutrient digestibilities and trypsin in pyloric caeca homogenate and intestinal content. , 1994, Comparative biochemistry and physiology. Part A, Physiology.