Abstract
The use of terrestrial invertebrates occurring in Siberia as a source of nutrients as an innovative form of new quality food production in North Asia is analysied. Two species, big slug Limacus flavus (Linnaeus, 1758) and rose chafer Cetonia aurata viridiventris Reitter, 1896 have been reared under laboratory conditions and prepared for nutrient analysis. Biomass have been taken from the instar stages of slugs and beetle larvae, animals have been killed by frozen and then presented for analysis. To determine the nutritive value, following macro- and micro- nutrients and dietary fibre have been revealed and determined from the biomass: В1 (thiamine), В2 (riboflavin), B3 (nicotinamide), B6 (pyridoxine), В9 (folacin), B12 (cyanocobalamin), Е (α- tocopherol), А (retinol palmitate), Fe, Se, Zn, Mn, Cu, Mg, F, lipid, protein, carbohydrate and chitin. In slugs and beetle larvae the mass fraction of protein is 20.6 and 20.8%, the fat percentage is 0.43 and 0.44%, and carbohydrate is 0.22 and 0.27%. Caloricity varied from 98 kilocalories in slugs to 96 in beetle larvae. All species are rich in magnesium (160 mg/100 g and 288 mg/100 g) and phosphorus (320 mg/100 g and 450 mg/100 g) (these elements are represented as macronutrients), and contains high level of iron (3.3 mg/100 g and 5.1 mg/100 g), copper (0.50 mg/100 g and 1.6 mg/100 g), selenium (0.0235 mg/100 g and 0.0334 mg/100 g), zinc (0.80 mg/100 g and 1.9 mg/100 g) and manganese (0.0076 mg/100 g and 0.0112 mg/100 g). Four vitamins detected, namely: А (0.0225 mg/100 g and 0.0337 mg/100 g), E (5.2 mg/100 g and 0.59 mg/100 g), В1 (2.5 mg/100 g) и В2 (5.2 mg/100 g and 0.59 mg/100 g). Almost completely lacking B3, B6, B9 and B12. Biomass both slugs and beetles is similar by nutrient composition and differs in presence of vitamin B3 in slugs, and 1.5 time higher vitamin A content in beetle larvae. The data revealed from the two terrestrial invertebrates show high level of natural nutrients, that could be used for food production, and in combination with not difficult raising hese species are perspective for farming in local conditions of different countries, excepting extremely hot and arid regions. Perspectives of terrestrial invertebrates farming for food production, safety aspects and comparative analysis with other edible species are discussed.
References
Belluco S, Losasso C, Maggioletti M, Alonzi CC, Paoletti MG, Ricci A (2013) Edible insects in a food safety and nutritional perspective: a critical review. Comprehensive Reviews in Food Science and Food Safety 12: 296–313. https://doi.org/10.1111/1541-4337.12014
DGE (Deutsche Gesellschaft für Ernährung) Die DGE/ÖGE-Referenzwerte für die Nährstoffzufuhr sind die Basis für die praktische Umsetzung einer vollwertigen Ernährung. https://www.dge.de/wissenschaft/referenzwerte
EFSA (European Food Safety Authority) (2015) Risk profile related to production and consumption of insects as food and feed. EFSA Journal 13 (10): 4257. https://doi.org/10.2903/j.efsa.2015.4257
EFSA (European Food Safety Authority) (2022) Safety of frozen and freeze and dried formulations of the lesser mealworm (Alphitobius diaperinus larva) as a Novel food pursuant to Regulation (EU) 2015/2283. EFSA Journal 20 (7): 7325. https://doi.org/10.2903/j.efsa.2022.7325
EFSA NDA Panel (EFSA Panel on Dietetic Products, Nutrition and Allergies) (2014) Scientific Opinion on Dietary Reference Values for niacin. EFSA Journal 12 (7): 3759. https://doi.org/10.2903/j.efsa.2014.3759
EFSA NDA Panel (EFSA Panel on Dietetic Products, Nutrition and Allergies) (2015a) Scientific Opinion on Dietary Reference Values for phosphorus. EFSA Journal 13 (7): 4185. https://doi.org/10.2903/j.efsa.2015.4185
EFSA NDA Panel (EFSA Panel on Dietetic Products, Nutrition and Allergies) (2015b) Scientific Opinion on Dietary Reference Values for magnesium. EFSA Journal 13 (7): 4186. https://doi.org/10.2903/j.efsa.2015.4186
EFSA NDA Panel (EFSA Panel on Dietetic Products, Nutrition and Allergies) (2015c) Scientific Opinion on Dietary Reference Values for copper. EFSA Journal 13 (10): 4253. https://doi.org/10.2903/j.efsa.2015.4253
EFSA NDA Panel (EFSA Panel on Dietetic Products, Nutrition and Allergies) (2015d) Scientific Opinion on Dietary Reference Values for iron. EFSA Journal 13 (10): 4254. https://doi.org/10.2903/j.efsa.2015.4254
EFSA Scientific Committee (2015) Scientific Opinion on a risk profile related to production and consumption of insects as food and feed. EFSA Journal 13 (10): 4257. https://doi.org/10.2903/j.efsa.2015.4257
Elhassan M, Wendin K, Olsson V, Langton M (2019) Quality Aspects of Insects as Food–Nutritional, Sensory, and Related Concepts. Foods 8(3): 95. https://doi.org/10.3390/foods8030095
EU Commission (2023) Commission Implementing Regulation (EU) 2023/58 of 5 January 2023 authorising the placing on the market of the frozen, paste, dried and powder forms of Alphitobius diaperinus larvae (lesser mealworm) as a novel food and amending Implementing Regulation (EU) 2017/2470. Document 32023R0058. http://data.europa.eu/eli/reg_impl/2023/58/oj
Fairweather-Tait SJ, Southon S (2003) Bioavailability of nutrients. In: Encyclopedia of Food Sciences and Nutrition. Academic Press, London, 478–484. https://doi.org/10.1016/B0-12-227055-X/00096-1
FAO (Food and Agriculture Organization) (2013) Dietary protein quality evaluation in human nutrition: report of an FAO Expert Consultation. Food and nutrition paper 92. FAO, Rome, 76 pp. https://www.fao.org/4/i3124e/i3124e.pdf
Finke MD, Rojo S, Roos N, Van Huis A, Yen AL (2015) The European food safety authority scientific opinion on a risk profile related to production and consumption of insects as food and feed. Journal of Insects as Food and Feed 1: 245–247. https://doi.org/10.3920/JIFF2015.x006
GOST 23042-2015 (2017) Meat and meat products. Methods of fat determination. Catalog of interstate standards. Standartinform, Moscow, 12 pp. https://docs.cntd.ru/document/1200133107
GOST 25011-2017 (2018) Meat and meat products. Protein determination methods. Catalog of interstate standards. Standartinform, Moscow, 17 pp. https://docs.cntd.ru/document/1200146783
GOST 31483-2012 (2013) Premixes. Determination of vitamins: B (thiaminchloride), B (riboflavin), B (pantothenic acid), B (nicotinic acid and nicotinamide), B (pyridoxine), B (folic acid), C (ascorbic acid) content by method of capillary electrophoresis. Catalog of interstate standards. Standartinform, Moscow, 20 pp. https://docs.cntd.ru/document/1200095471
GOST 31675-2012 (2020) Feeds. Methods for determination of crude fibre content with intermediate filtration. Catalog of interstate standards. Standartinform, Moscow, 10 pp. https://internet-law.ru/gosts/gost/52702
GOST 32009-2013 (2014) Meat and meat products. Spectrophotometric method for determination of total phosphorous content. Catalog of interstate standards. Standartinform, Moscow, 13 pp. https://docs.cntd.ru/document/1200104976
GOST 4011-72 (1974) Driking water. Methods for determination of total iron. Catalog of interstate standards. Standartinform, Moscow, 8 pp. https://docs.cntd.ru/document/1200008210
GOST EN 12822-2014 (2016) Foodstuffs. Determination of vitamin E (alpha-, beta-, gamma- and delta-tocopherols) content by high performance liquid chromatography. Catalog of interstate standards. Standartinform, Moscow, 16 pp. https://docs.cntd.ru/document/1200112673
GOST EN 14122-2013 (2015) Foodstuffs. Determination of vitamin B by HPLC. Catalog of interstate standards. Standartinform, Moscow, 24 pp. https://docs.cntd.ru/document/1200109214
GOST EN 14152-2013 (2015) Foodstuffs. Determination of vitamin B2 by HPLC. Catalog of interstate standards. Standartinform, Moscow,16 pp. https://docs.cntd.ru/document/1200109207
GOST EN 14164-2014 (2017) Foodstuffs. Determination of vitamin B6 by high performance chromatography. Catalog of interstate standards. Standartinform, Moscow, 18 pp. https://docs.cntd.ru/document/1200134856
GOST ISO 20634-2018 (2019) Infant formula and adult nutritionals. Determination of vitamin B12 by reversed phase high performance liquid chromatography. Catalog of interstate standards. Standartinform, Moscow, 20 pp. https://docs.cntd.ru/document/1200160124
GOST Р 53747-2009 (2011) Poultry meat, edible offal and semi-processed products. Methods for organoleptic and physico-chemical analysis. Catalog of national standards. Standartinform, Moscow, 29 pp. https://docs.cntd.ru/document/1200078391
GOST Р 54635-2011 (2013) Functional food products. Method of vitamin А determination. Catalog of national standards. Standartinform, Moscow, 16 pp. https://docs.cntd.ru/document/1200091389
Hanboonsong Yu, Jamjanya T, Durst PB (2013) Six-legged livestock: edible insect farming, collection and marketing in Thailand Bangkok. Food and agriculture organization of the United Nations regional office for Asia and the Pacific, Bangkok, 58 pp. https://www.fao.org/3/i3246e/i3246e00.htm
Hayashida PY, da Silva Junior PI (2021) Insights into Antimicrobial Peptides from Limacus flavus Mucus. Current Microbiology 78(8): 2970–2979. https://doi.org/10.1007/s00284-021-02552-3
Heaney RP (2001) Factors Influencing the Measurement of Bioavailability, Taking Calcium as a Model. The Journal of Nutrition 131(4): 1344–1348. https://doi.org/10.1093/jn/131.4.1344S
Hebert MF (2013) 3 – Impact of Pregnancy on Maternal Pharmacokinetics of Medications. Clinical Pharmacology During Pregnancy 20(3): 17–39. https://doi.org/10.1016/B978-0-12-386007-1.00003-9
Keil C, Grebenteuch S, Kröncke N, Kulow, F, Pfeif S, Kanzler C, Rohn S, Boeck G, Benning R, Haase H (2022) Systematic Studies on the Antioxidant Capacity and Volatile Compound Profile of Yellow Mealworm Larvae (T. molitor L.) under Different Drying Regimes. Insects 13: 166. https://doi.org/10.3390/insects13020166
Lahteenmaki-Uutela A, Grmelova N (2016) European law on insects in food and feed. European Food and Feed Law Review 11: 2–8. https://www.jstor.org/stable/43958606
Lepski S, Brockmeyer J (2013) Impact of dietary factors and food processing on food allergy. Molecular Nutrition and Food Research 57(1): 145–152. https://doi.org/10.1002/mnfr.201200472
Leser S (2013) The 2013 FAO report on dietary protein quality evaluation in human nutrition: Recommendations and implications. Nutrition Bulletin 38: 421–428. https://doi.org/10.1111/nbu.12063
Lumsa-ad C (2001) A study on the species and the nutrition values of edible insects in Upper Southern Thailand. Khon Kaen Agriculture Journal 29(1): 45–49. [In Thai]
Marze S (2013) Bioaccessibility of Nutrients and Micronutrients from Dispersed Food Systems: Impact of the Multiscale Bulk and Interfacial Structures. Critical Reviews in Food Science and Nutrition 53(1): 76–108. https://doi.org/10.1080/10408398.2010.525331
Melis R, Braca A, Sanna R, Spada S, Mulas G, Fadda ML, Anedda R (2019) Metabolic response of yellow mealworm larvae to two alternative rearing substrates. Metabolomics 15(8): 113. https://doi.org/10.1007/s11306-019-1578-2
Mielgo-Ayuso J, Aparicio-Ugarriza R, Olza J, Aranceta-Bartrina J, Gil Á, Ortega RM, Serra-Majem L, Varela-Moreiras G, González-Gross M (2018) Dietary Intake and Food Sources of Niacin, Riboflavin, Thiamin and Vitamin B6 in a Representative Sample of the Spanish Population. The ANIBES Study. Nutrients 10: 846. https://doi.org/10.3390/nu10070846
Nowak V, Persijn D, Rittenschober D, Charrondiere UR (2016) Review of food composition data for edible insects. Food Chemistry 193: 39–46. https://doi.org/10.1016/j.food-chem.2014.10.114
Oonincx DGAB, Van der Poel AFB (2011) Effects of diet on the chemical composition of migratory locusts (Locusta migratoria). Zoo Biology 30: 9–16. https://doi.org/10.1002/zoo.20308
Rattanapan R (2000) Edible insect diversity and cytogenetic studies on short-tail crickets (Genus Brachytrupes) in northeastern Thailand. Dissertation for the degree of Master of Science, Khon Kaen University, Thailand. [In Thai]
Regulation (EC) (2004) No 852/2004 of the European Parliament and of the Council of 29 April 2004 on the hygiene of foodstuffs. Official Journal of the European Communities L 139: 1–54. http://data.europa.eu/eli/reg/2004/852/oj
Regulation (EC) (2009) Regulation No 1069/2009 of the European Parliament and of the Council of 21 October 2009 laying down health rules as regards animal by-products and derived products not intended for human consumption and repealing Regulation (EC) No 1774/2002 (Animal by-products Regulation). Official Journal of the European Union L 300: 1–33. http://data.europa.eu/eli/reg/2009/1069/oj
Regulation (EU) (2015) No 2015/2283 of the European Parliament and of the Council of 25 November 2015. Official Journal of the European Union L 327: 1–22. http://data.europa.eu/eli/reg/2015/2283/oj
Rumpold BA, Schlüter OK (2013a) Potential and challenges of insects as an innovative source for food and feed production. Innovative Food Science & Emerging Technologies 17: 1–11. https://doi.org/10.1016/j.ifset.2012.11.005
Rumpold BA, Schlüter OK (2013b) Nutritional composition and safety aspects of edible insects. Molecular Nutrition Food Research 57: 802–823. https://doi.org/10.1002/mnfr.201200735
Sandstead HH, Au W (2007) Zinc*. In: Nordberg GF, Fowler, BA, Nordberg, M, Friberg LT (Eds) Handbook on the Toxicology of Metals. Academic Press, Amsterdam, 925–947. https://doi.org/10.1016/b978-012369413-3/50102-6
Schlussbericht zu IGF-Vorhaben Nr. 18235 N (2020) Funktionsmuster einer industriellen Produktions- und Fraktionierungsanlage (Fett + Protein) von Insekten. Berichtszeitraum 01.10.2015–30.09.2018. Internationale Forschungsgemeinschaft Futtermitteltechnik eV, Hochschule Bremerhaven, Labor für Lebensmittelchemie, 86 pp. https://www.iff-braunschweig.de/wp-content/uploads/2020/01/IGF-18235-N-Funktionsmuster.pdf
Siemianowska E, Kosewska, A, Aljewicz M, Skibniewska K, Polak-Juszczak L, Jarocki A, Jędras M (2013) Larvae of mealworm (Tenebrio molitor L.) as European novel food. Agricultural Sciences 4 (6): 287–291. https://doi.org/10.4236/as.2013.46041
Solomons NW, Au W (2003) Zinc/Physiology. In: Encyclopedia of Food Sciences and Nutrition. Academic Press, London, 6272–6277. https://doi.org/10.1016/b0-12-227055-x/01309-2
Thompson R, Cheney S (1996) Raising snails. The Alternative Farming Systems Information Center, National Agricultural Library. US Department of Agriculture, Special Reference Briefs Series no. SRB 96-05, 29 pp. https://naldc.nal.usda.gov/download/7083485/PDF (accessed on 23.12.2022)
Tshernyshev SE, Babenko AS, Babkina IB, Baghirov RT-O, Modyaeva VP, Morozova MD, Skriptcova KE, Subbotina EYu, Shcherbakov MV, Simakova AV (2024) Invertebrates of Siberia, a potential source of animal protein for innovative food and feed production. 5. Changes of nutrient composition in worms and crickets after particular enrichment of feeding substrate. Euroasian Entomological Journal 23(5): 135–145. https://doi.org/10.15298/euroasentj.23.05.10
Tshernyshev SE, Babkina IB, Modyaeva VP, Morozova MD, Subbotina EYu, Shcherbakov MV, Simakova AV (2022) Invertebrates of Siberia, a potential source of animal protein for innovative food production. 1. The keelback slugs (Gastropoda: Limacidae). Acta Biologica Sibirica 8: 749–762. https://doi.org/10.14258/abs.v8.e47
Tshernyshev SE, Baghirov RT-O, Modyaeva VP, Morozova MD, Skriptcova KE, Subbotina EYu, Shcherbakov MV, Simakova AV (2023a) Invertebrates of Siberia, a potential source of animal protein for innovative human food production. 3. Principles of biomass nutrient composition design. Euroasian Entomological Journal 22 (5): 246–255. https://doi.org/10.15298/euroasentj.22.05.03
Tshernyshev SE, Baghirov RT-O, Modyaeva VP, Morozova MD, Skriptcova KE, Subbotina EYu, Shcherbakov MV, Simakova AV (2023b) Invertebrates of Siberia, a potential source of animal protein for innovative food production. 4. New method of protein food and feed products generation. Euroasian Entomological Journal. 22 (6): 285–290. https://doi.org/10.15298/euroasentj.22.06.1
Turck D, Castenmiller J, De Henauw S, Hirsch-Ernst KI, Kearney J, Maciuk A, Mangelsdorf I, McArdle HJ, Naska A, Pelaez (2021) Safety of frozen and dried formulations from migratory locust (Locusta migratoria) as a Novel food pursuant to Regulation (EU) 2015/2283. EFSA Journal 19(7): 6667. https://efsa.onlinelibrary.wiley.com/doi/full/10.2903/j.efsa.2021.6667
Tutelyan VA, Baturin AK, Gapparov MG, Kaganov BS, Kon IYa, Mazo VK, Baeva VS, Bessonov VV, Vasilev AV, Volkova LYu, Vrzhesinskaya OA, Gmoshinskaya MV, Zhminchenko VM, Zilova IS, Keshabyanc EE, Kodencova VM, Kravchenko LV, Kulakova SN, Lashneva NV, Pogozheva AV, Safronova AM, Sokolov AI, Spirichev VB, Xotimchenko SA, Shilina NM, Baranov AA, Borovik TE, Onishhenko GG, Suxanov BP, Grigorev AI, Korovina NA, Sorvacheva TN (2009) Normy fiziologicheskix potrebnostej v energii i pishhevyx veshhestvax dlya razlichnyx grupp naseleniya rossijskoj federacii. [The norms of physiological requirements in energy and nutrients for various of population in Russian Federation]. Metodicheskie rekomendacii MR 2.3.1.2432-08. Federalnyj centr gigieny i epidemiologii rospotrebnadzora RF, Moskva, 30 pp. https://docs.cntd.ru/document/1200076084
Tutelyan VA, Nikityuk DB, Aksenov IV, Baturin AK, Bessonov VV, Vorobyova VM, Vorobyova IS, Vrzhesinskaya OA, Vybornaya KV, Gmoshinskii IV, Gmoshinskaya MV, Zhilinskaya NV, Kambarov AO, Keshabyants EE, Kobelkova IV, Kodentsova VM, Koshechkina AS, Kochetkova AA, Kravchenko LV, Kudryavtseva KV, Lashneva NV, Mazo VK, Makarenko MA, Martinchik AN, Pavlovskaya EV, Perova IB, Pogozheva AV, Pyrieva EA, Rylina EV, Sidorova YuS, Safronova AI, Safronova AM, Smirnova EA, Sokolov AI, Starodubova AV, Tarmaeva IYu, Hotimchenko SA, Sharafetdinov HH, Shilina NM, Eller KI, Popova AYu, Brarina IN, Smolenskii VYu, Mishina AL, Shevkun IG, Yanovskaya GV, Salagai OO, Skvortsova VI, Onishchenko GG, Suhanov BP, Elizarova EV, Novikova II, Romanenko SL, Shevelyova SA, Efimochkina NR, Dyatlov IA, Kafarskaya LI, Priputnevich TV (2021) Normy fiziologicheskih potrebnostei v energii i pishchevyh veshchestvah dlya razlichnyh grupp naseleniya Rossiiskoi Federacii. [The norms of physiological requirements in energy and nutrients for various of population in Russian Federation]. Metodicheskie rekomendacii MR 2.3.1.0253-21. Federalnyi centr gigieny i epidemiologii Rospotrebnadzora RF, Moskva, 57 pp. https://www.rospotrebnadzor.ru/documents/details.php?ELEMENT_ID=18979
Van der Fels-Klerx HJ, Camenzuli L, Van der Lee MK, Oonincx DGAB (2016) Uptake of Cadmium, Lead and Arsenic by Tenebrio molitor and Hermetia illucens from Contaminated Substrates. PLOS ONE 11(11): e0166186. https://doi.org/10.1371/journal.pone.0166186
Van der Spiegel M, Noordam M, Van der Fels-Klerx HJ (2013) Safety of novel protein sources (Insects, Microalgae, Seaweed, Duckweed, Rapeseed) and legislative aspects for their application in food and feed production. Comprehensive Reviews in Food Science and Food Safety 12 (6): 662–678. https://doi.org/10.1111/1541-4337.12032
Van Huis A (2013) Potential of insects as food and feed in assuring food security. Annual Review of Entomology 58 (1): 563–583. https://doi.org/10.1146/annurev-ento-120811-153704
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. FAO forestry paper 171. Wageningen UP for better life, Rome, 190 pp. https://www.fao.org/3/i3253e/i3253e.pdf
Van Peer M, Frooninckx L, Coudron C, Berrens S, Álvarez C, Deruytter D, Verheyen G, Van Miert S (2021) Valorisation Potential of Using Organic Side Streams as Feed for Tenebrio molitor, Acheta domesticus and Locusta migratoria. Insects 12 (9): 796. https://doi.org/10.3390/insects12090796
Van Raamsdonk LWD, Van der Fels-Klerx HJ, De Jong J (2017) New feed ingredients: the insect opportunity. Food Additives & Contaminants: Part A 34 (8): 1384–1397. https://doi.org/10.1080/19440049.2017.1306883
Verhoeckx KCM, Broekhoven S, Hartog-Jager CF, Gaspari M, Govardus AH de Jong, Wichers HJ, Van Hoffen E, Houben GF, Knulst AC (2014) House dust mite (Der p 10) and crustacean allergic patients may react to food containing Yellow mealworm proteins. Food and Chemical Toxicology 65: 364–373. https://doi.org/10.1016/j.fct.2013.12.049
Zagrobelny M, Dreon AL, Gomiero T, Marcazzan GL, GlaringMA, MøLler BL, Paoletti MG (2009). Toxic Moths: Source of a Truly Safe Delicacy. Journal of Ethnobiology 29 (1): 64–76. https://doi.org/10.2993/0278-0771-29.1.64
Zielińska E, Baraniak B, Karaś M, Rybczyńska K, Jakubczyk A (2015) Selected species of edible insects as a source of nutrient composition. Food Research International 77: 460– 466. https://doi.org/10.1016/j.foodres.2015.09.008
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