Replacing fish meal with insect meal in the diet of Atlantic salmon (Salmo salar) does not impact the amount of contaminants in the feed and it lowers accumulation of arsenic in the fillet

References

• Almela C, Jesús Clemente M, Vélez D, Montoro R. 2006. Total arsenic, inorganic arsenic, lead and cadmium contents in edible seaweed sold in Spain. Food Chem Toxicol. 44(11):1901–1908.
   PubMed Web of Science ®Google Scholar
• Atobatele OE, Olutona GO. 2015. Distribution of three non-essential trace metals (Cadmium, Mercury and Lead) in the organs of fish from Aiba reservoir, Iwo, Nigeria. Toxicol Rep. 2:896–903.
   PubMed Web of Science ®Google Scholar
• Barroso FG, de Haro C, Sanchez-Muros MJ, Venegas E, Martinez-Sanchez A, Perez-Banon C. 2014. The potential of various insect species for use as food for fish. Aquaculture. 422:193–201.
   Web of Science ®Google Scholar
• Belghit I, Liland NS, Gjesdal P, Biancarosa I, Menchetti E, Li Y, Waagbø R, Krogdahl Å, Lock E-J. 2018a. Black soldier fly larvae meal can replace fish meal in diets of sea-water phase Atlantic salmon (Salmo salar). Aquaculture. 503:609–619.
   Web of Science ®Google Scholar
• Belghit I, Liland NS, Waagbø R, Biancarosa I, Pelusio N, Li Y, Krogdahl Å, Lock E-J. 2018b. Potential of insect-based diets for Atlantic salmon (Salmo salar). Aquaculture. 491:72–81.
   Web of Science ®Google Scholar
• Berntssen MHG, Julshamn K, Lundebye A-K. 2010. Chemical contaminants in aquafeeds and Atlantic salmon (Salmo salar) following the use of traditional- versus alternative feed ingredients. Chemosphere. 78(6):637–646.
   PubMed Web of Science ®Google Scholar
• Biancarosa I, Belghit I, Bruckner CG, Liland NS, Waagbø R, Amlund H, Heesch S, Lock E-J. 2018a. Chemical characterization of 21 species of marine macroalgae common in Norwegian waters: benefits of and limitations to their potential use in food and feed. J Sci Food Agric. 98(5):2035–2042.
   PubMed Web of Science ®Google Scholar
• Biancarosa I, Liland NS, Biemans D, Araujo P, Bruckner CG, Waagbø R, Torstensen BE, Lock E-J, Amlund H. 2018b. Uptake of heavy metals and arsenic in black soldier fly (Hermetia illucens) larvae grown on seaweed-enriched media. J Sci Food Agric. 98(6):2176–2183.
   PubMed Web of Science ®Google Scholar
• Borgogno M, Dinnella C, Iaconisi V, Fusi R, Scarpaleggia C, Schiavone A, Monteleone E, Gasco L, Parisi G. 2017. Inclusion of Hermetia illucens larvae meal on rainbow trout (Oncorhynchus mykiss) feed: effect on sensory profile according to static and dynamic evaluations. J Sci Food Agric. 97(10):3402–3411.
   PubMed Web of Science ®Google Scholar
• Camenzuli L, Van Dam R, De Rijk T, Andriessen R, Van Schelt J, Van der Fels-Klerx JH. 2018. Tolerance and excretion of the mycotoxins aflatoxin B1, zearalenone, deoxynivalenol, and ochratoxin A by alphitobius diaperinus and hermetia illucens from contaminated substrates. Toxins. 10(2):91.
   PubMed Web of Science ®Google Scholar
• Charlton AJ, Dickinson M, Wakefield ME, Fitches E, Kenis M, Han R, Zhu F, Kone N, Grant M, Devic E, et al. 2015. Exploring the chemical safety of fly larvae as a source of protein for animal feed. J Insects Food Feed. 1(1):7–16.
   Web of Science ®Google Scholar
• Díaz O, Tapia Y, Muñoz O, Montoro R, Velez D, Almela C. 2012. Total and inorganic arsenic concentrations in different species of economically important algae harvested from coastal zones of Chile. Food Chem Toxicol. 50(3–4):744–749.
   PubMed Web of Science ®Google Scholar
• Diener S, Zurbrügg C, Tockner K. 2015. Bioaccumulation of heavy metals in the black soldier fly, Hermetia illucens and effects on its life cycle. J Insects Food Feed. 1(4):261–270.
   Web of Science ®Google Scholar
• Duinker A, Roiha IS, Amlund H, Dahl L, Lock E-J, Kögel T, Måge A, Lunestad BT 2016. Potential risks posed by macroalgae for application as feed and food-a Norwegian perspective. Technical report National Institute of Nutrition and Seafood Research (NIFES).
   Google Scholar
• Edmonds JS, Francesconi KA. 1987. Transformations of arsenic in the marine environment. Experientia. 43(5):553–557.
   PubMedGoogle Scholar
• Edmonds JS, Francesconi KA. 2003. Organoarsenic compounds in the marine environment. New Jersey (USA): John Wiley & Sons, Ltd; p. 195–222.
   Google Scholar
• Edmonds JS, Shibata Y, Francesconi KA, Rippingale RJ, Morita M. 1997. Arsenic transformations in short marine food chains studied by HPLC‐ICP MS. Appl Organomet Chem. 11(4):281–287.
   Web of Science ®Google Scholar
• [EFSA] European Food Safety Authority. 2004. Opinion of the scientific panel on contaminants in the food chain [CONTAM] related to fluorine as undesirable substance in animal feed. EFSA J.
   PubMedGoogle Scholar
• [EFSA] European Food Safety Authority. 2009. Scientific opinion on arsenic in food EFSA panel on contaminants in the food chain (CONTAM). EFSA J. 7(10):1351.
   Google Scholar
• [EFSA] European Food Safety Authority. 2015. Risk profile related to production and consumption of insects as food and feed. EFSA J. 13(10):4257.
   PubMed Web of Science ®Google Scholar
• [EU] European Union. 2002. Directive 2002/32/EC of the European Parliament and the Council of 7 May 2002 on undesirable substances in animal feed.
   Google Scholar
• [EU] European Union. 2006. Commission Recommendation of 17 August 2006 on the presence of deoxynivalenol, zearalenone, ochratoxin A, T-2 and HT-2 and fumonisins in products intended for animal feeding.
   Google Scholar
• [EU] European Union. 2017. Commission Regulation (EU) 2017/893 of 24 May 2017 amending Annexes I and IV to Regulation (EC) No 999/2001 of the European Parliament and of the Council and Annexes X, XIV and XV to Commission Regulation (EU) No 142/2011 as regards the provisions on processed animal protein.
   Google Scholar
• Feldmann J, Krupp EM. 2011. Critical review or scientific opinion paper: arsenosugars—a class of benign arsenic species or justification for developing partly speciated arsenic fractionation in foodstuffs? Anal Bioanal Chem. 399(5):1735–1741.
   PubMed Web of Science ®Google Scholar
• Francesconi KA, Edmonds JS. 1998. Arsenic species in marine samples. Croatica Chemica Acta. 71(2):343–359.
   Web of Science ®Google Scholar
• Francesconi KA, Kuehnelt D. 2004. Determination of arsenic species: A critical review of methods and applications, 2000–2003. Analyst. 129(5):373–395.
   PubMed Web of Science ®Google Scholar
• Gao Q, Wang X, Wang W, Lei C, Zhu F. 2017. Influences of chromium and cadmium on the development of black soldier fly larvae. Environ Sci Pollut Res. 24(9):8637–8644.
   PubMed Web of Science ®Google Scholar
• Handy RD. 1992. The assessment of episodic metal pollution. II. The effects of cadmium and copper enriched diets on tissue contaminant analysis in rainbow trout (Oncorhynchus mykiss). Arch Environ Contam Toxicol. 22(1):82–87.
   PubMed Web of Science ®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.
   Web of Science ®Google Scholar
• Hwang YO, Park SG, Park GY, Choi SM, Kim MY. 2010. Total arsenic, mercury, lead, and cadmium contents in edible dried seaweed in Korea. Food Addit Contam: Part B. 3(1):7–13.
   PubMed Web of Science ®Google Scholar
• Johnsen CA, Hagen Ø, Adler M, Jönsson E, Kling P, Bickerdike R, Solberg C, Björnsson BT, Bendiksen EÅ. 2011. Effects of feed, feeding regime and growth rate on flesh quality, connective tissue and plasma hormones in farmed Atlantic salmon (Salmo salar L.). Aquaculture. 318(3):343–354.
   Web of Science ®Google Scholar
• Julshamn K, Maage A, Norli HS, Grobecker KH, Jorhem L, Fecher P, Dowell D. 2013. Determination of arsenic, cadmium, mercury, and lead in foods by pressure digestion and inductively coupled plasma/mass spectrometry: first action 2013.06. J AOAC Int. 96(5):1101–1102.
   PubMed Web of Science ®Google Scholar
• Julshamn K, Nilsen BM, Frantzen S, Valdersnes S, Maage A, Nedreaas K, Sloth JJ. 2012. Total and inorganic arsenic in fish samples from Norwegian waters. Food Addit Contam: Part B. 5(4):229–235.
   PubMed Web of Science ®Google Scholar
• Kaushik SJ, Medale F, Fauconneau B, Blanc D. 1989. Effect of digestible carbohydrates on protein/energy utilization and on glucose metabolism in rainbow trout (Salmo gairdneri R.). Aquaculture. 79(1):63–74.
   Web of Science ®Google Scholar
• Kjellevold Malde M, Bjorvatn K, Julshamn K. 2001. Determination of fluoride in food by the use of alkali fusion and fluoride ion-selective electrode. Food Chem. 73(3):373–379.
   Web of Science ®Google Scholar
• Kouřimská L, Adámková A. 2016. Nutritional and sensory quality of edible insects. Nfs J. 4:22–26.
   Google Scholar
• Liland NS, Biancarosa I, Araujo P, Biemans D, Bruckner CG, Waagbø R, Torstensen BE, Lock E-J. 2017. Modulation of nutrient composition of black soldier fly (Hermetia illucens) larvae by feeding seaweed-enriched media. PLoS One. 12(8):e0183188.
   PubMed Web of Science ®Google Scholar
• Lock E-J, Biancarosa I, Gasco L. 2018. Insects as raw materials in compound feed for aquaculture. In: Halloran A, Flore R, Vantomme P, Roos N, editors. Edible insects in sustainable food systems. Cham (UK): Springer International Publishing; p. 263–276.
   Google Scholar
• Lock E-J, Arsiwalla T, Waagbø R. 2016. Insect larvae meal as an alternative source of nutrients in the diet of Atlantic salmon (Salmo salar) postsmolt. Aquac Nutr. 22(6):1202–1213.
   Web of Science ®Google Scholar
• Lundebye A-K, Lock E-J, Rasinger JD, Nøstbakken OJ, Hannisdal R, Karlsbakk E, Wennevik V, Madhun AS, Madsen L, Graff IE, et al. 2017. Lower levels of Persistent Organic Pollutants, metals and the marine omega 3-fatty acid DHA in farmed compared to wild Atlantic salmon (Salmo salar). Environ Res. 155:49–59.
   Google Scholar
• Maehre HK, Malde MK, Eilertsen KE, Elvevoll EO. 2014. Characterization of protein, lipid and mineral contents in common Norwegian seaweeds and evaluation of their potential as food and feed. J Sci Food Agric. 94(15):3281–3290.
   PubMed Web of Science ®Google Scholar
• Magalhães R, Sánchez-López A, Leal RS, Martínez-Llorens S, Oliva-Teles A, Peres H. 2017. Black soldier fly (Hermetia illucens) pre-pupae meal as a fish meal replacement in diets for European seabass (Dicentrarchus labrax). Aquaculture. 476:79–85.
   Web of Science ®Google Scholar
• Makkar HPS, Tran G, Heuzé V, Ankers P. 2014. State-of-the-art on use of insects as animal feed. Anim Feed Sci Technol. 197:1–33.
   Web of Science ®Google Scholar
• Matejova I, Svobodova Z, Vakula J, Mares J, Modra H. 2017. Impact of mycotoxins on aquaculture fish species: A review. J World Aquac Soc. 48(2):186–200.
   Web of Science ®Google Scholar
• Nogales-Mérida S, Gobbi P, Józefiak D, Mazurkiewicz J, Dudek K, Rawski M, Kierończyk B, Józefiak A. 2018. Insect meals in fish nutrition. Rev Aquacult. doi:10.1111/raq.12281
   Web of Science ®Google Scholar
• Poma G, Cuykx M, Amato E, Calaprice C, Focant JF, Covaci A. 2017. Evaluation of hazardous chemicals in edible insects and insect-based food intended for human consumption. Food Chem Toxicol. 100:70–79.
   PubMed Web of Science ®Google Scholar
• R Core Team. 2011. R: a language and environment for statistical computing. Vienna (Austria): R Foundation for Statistical Computing. http://www.R-project.org/.
   Google Scholar
• Renna M, Schiavone A, Gai F, Dabbou S, Lussiana C, Malfatto V, Prearo M, Capucchio MT, Biasato I, Biasibetti E, et al. 2017. 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. J Anim Sci Biotechnol. 8(1):57.
   PubMed Web of Science ®Google Scholar
• Ronan JM, Stengel DB, Raab A, Feldmann J, O'Hea L, Bralatei E, McGovern E. 2017. High proportions of inorganic arsenic in laminaria digitata but not in ascophyllum nodosum samples from Ireland. Chemosphere. 186:17–23.
   PubMed Web of Science ®Google Scholar
• Rose M, Lewis J, Langford N, Baxter M, Origgi S, Barber M, MacBain H, Thomas K. 2007. Arsenic in seaweed—forms, concentration and dietary exposure. Food Chem Toxicol. 45(7):1263–1267.
   PubMed Web of Science ®Google Scholar
• Scheibelberger R, Axmann S, Adler A, Jäger H. 2017. Impact of substrate contamination with mycotoxins, heavy metals and pesticides on the growth performance and composition of black soldier fly larvae (Hermetia illucens) for use in the feed and food value chain AU - Purschke, Benedict. Food Addit Contam: Part A. 34(8):1410–1420.
   Google Scholar
• Sele V, Sanden M, Berntssen MHG, Lunestad BT, Espe M, Lie KK, Amlund H, Lundebye A-K, Hemre G-I, Waagbo R, et al. 2018. Program for overvåking av fiskefôr – Årsrapport for prøver innsamlet i 2017. Institute of Marine Research. https://www.imr.no.
   Google Scholar
• Sele V, Sloth JJ, Holmelid B, Valdersnes S, Skov K, Amlund H. 2014. Arsenic-containing fatty acids and hydrocarbons in marine oils – determination using reversed-phase HPLC–ICP-MS and HPLC–qTOF-MS. Talanta. 121:89–96.
   PubMed Web of Science ®Google Scholar
• Sele V, Sloth JJ, Julshamn K, Skov K, Amlund H. 2015. A study of lipid- and water-soluble arsenic species in liver of Northeast Arctic cod (Gadus morhua) containing high levels of total arsenic. J Trace Elem Med Biol. 30:171–179.
   PubMed Web of Science ®Google Scholar
• Sissener NH, Julshamn K, Espe M, Lunestad BT, Hemre GI, Waagbø R, Måge A. 2013. Surveillance of selected nutrients, additives and undesirables in commercial Norwegian fish feeds in the years 2000–2010. Aquac Nutr. 19(4):555–572.
   Web of Science ®Google Scholar
• Sloth JJ, Julshamn K, Lundebye A-K. 2005a. Total arsenic and inorganic arsenic content in Norwegian fish feed products. Aquac Nutr. 11(1):61–66.
   Web of Science ®Google Scholar
• Sloth JJ, Larsen EH, Julshamn K. 2003. Determination of organoarsenic species in marine samples using gradient elution cation exchange HPLC-ICP-MS. J Anal At Spectrom. 18(5):452–459. doi: 10.1039/B300508A
   Web of Science ®Google Scholar
• St-Hilaire S, Sheppard C, Tomberlin JK, Irving S, Newton L, McGuire MA, Mosley EE, Hardy RW, Sealey W. 2007. Fly prepupae as a feedstuff for rainbow trout, oncorhynchus mykiss. J World Aquac Soc. 38(1):59–67.
   Web of Science ®Google Scholar
• Tocher DR. 2010. Fatty acid requirements in ontogeny of marine and freshwater fish. Aquacult Res. 41(5):717–732.
   Web of Science ®Google Scholar
• Torstensen BE, Frøyland L, Lie Ø. 2004. Replacing dietary fish oil with increasing levels of rapeseed oil and olive oil – effects on Atlantic salmon (Salmo salar L.) tissue and lipoprotein lipid composition and lipogenic enzyme activities. Aquac Nutr. 10(3):175–192.
   Web of Science ®Google Scholar
• Van Broekhoven S, Gutierrez JM, De Rijk TC, De Nijs WCM, Van Loon JJA. 2017. Degradation and excretion of the Fusarium toxin deoxynivalenol by an edible insect, the Yellow mealworm (Tenebrio molitor L.). World Mycotoxin J. 10(2):163–169.
   Web of Science ®Google Scholar
• Van den Berg M, Birnbaum LS, Denison M, De Vito M, Farland W, Feeley M, Fiedler H, Hakansson H, Hanberg A, Haws L, et al. 2006. The 2005 World Health Organisation re-evaluation of human and mammalian toxic equivalency factors for dioxins and dioxin-like compounds. Toxicol Sci. 93(2):223–241.
   PubMed Web of Science ®Google Scholar
• van der Fels-Klerx H, Camenzuli L, Van Der Lee M, Oonincx D. 2016. Uptake of cadmium, lead and arsenic by tenebrio molitor and hermetia illucens from contaminated substrates. PLoS One. 11(11):e0166186.
   PubMed Web of Science ®Google Scholar
• van Huis A. 2013. Potential of insects as food and feed in assuring food security. Annu Rev Entomol. 58:563–583.
   PubMed Web of Science ®Google Scholar
• Villares R, Puente X, Carballeira A. 2002. Seasonal variation and background levels of heavy metals in two green seaweeds. Environ Pollut. 119(1):79–90.
   PubMed Web of Science ®Google Scholar
• Yamada M, Yamamoto K, Ushihara Y, Kawai H. 2007. Variation in metal concentrations in the brown alga undaria pinnatifida in Osaka Bay, Japan. Phycol Res. 55(3):222–230.
   Web of Science ®Google Scholar