Abstract
Mealworms are commercially reared on diets comprising of mixed grains. Substituting grains with agro-food industry by-products creates opportunities to valorize by-products and lowers the cost of insect rearing practices. In this study, three by-products (mushroom spent corn stover, highly denatured soybean meal, and spirit distillers’ grains) as treatments and wheat bran as control were used to rear mealworms. For growth performance, mealworms dry weights reared on three by-products were 53–67% of control. Feed conversion and utilization ratios ranged from 36 to 45% and 50 to 57% of control, respectively. For nutritional profile, protein and fat fractions ranged from 70 to 76% and 6 to 12% of mealworm dry weight, respectively. Leucine, lysine, methionine + cysteine, threonine, and valine were the limiting amino acids comparing with FAO/WHO requirements. The major fatty acids were linoleic acid (C18:2, 30–38%), oleic acid (C18:1, 24–34%), and palmitic acid (C16:0, 14–17%). The comparable nutritional profile demonstrated the potential to rear mealworms using these three cheap by-products. The results provide a reference for insect farmers to formulate the diets for obtaining specific insect products with desired nutrient composition.
Similar content being viewed by others
References
Zielinska E, Baraniak B, Karas M, Rybczynska K, Jakubczyk A (2015) Selected species of edible insects as a source of nutrient composition. Food Res Int 77:460–466. https://doi.org/10.1016/j.foodres.2015.09.008
Van Broekhoven S, Oonincx DG, Van Huis A, Van Loon JJ (2015) Growth performance and feed conversion efficiency of three edible mealworm species (Coleoptera: Tenebrionidae) on diets composed of organic by-products. J Insect Physiol 73:1–10. https://doi.org/10.1016/j.jinsphys.2014.12.005
Naziri E, Nenadis N, Mantzouridou FT, Tsimidou MZ (2014) Valorization of the major agrifood industrial by-products and waste from Central Macedonia (Greece) for the recovery of compounds for food applications. Food Res Int 65:350–358. https://doi.org/10.1016/j.foodres.2014.09.013
Li M, Eskridge K, Liu E, Wilkins M (2019) Enhancement of polyhydroxybutyrate (PHB) production by 10-fold from alkaline pretreatment liquor with an oxidative enzyme-mediator-surfactant system under Plackett-Burman and central composite designs. Bioresour Technol 281:99–106. https://doi.org/10.1016/j.biortech.2019.02.045
Ding C, Wang X, Li M (2019) Evaluation of six white-rot fungal pretreatments on corn stover for the production of cellulolytic and ligninolytic enzymes, reducing sugars, and ethanol. Appl Microbiol Biotechnol. https://doi.org/10.1007/s00253-019-09884-y
Li M, Eskridge KM, Wilkins MR (2019) Optimization of polyhydroxybutyrate production by experimental design of combined ternary mixture (glucose, xylose and arabinose) and process variables (sugar concentration, molar C:N ratio). Bioprocess Biosystems Eng 1:12. https://doi.org/10.1007/s00449-019-02146-1
Frederick N, Li M, Carrier DJ, Buser MD, Wilkins MR (2016) Switchgrass storage effects on the recovery of carbohydrates after liquid hot water pretreatment and enzymatic hydrolysis. AIMS Bioeng 3(3):389–399. https://doi.org/10.3934/bioeng.2016.3.389
Zhao C, Zou Z, Li J, Jia H, Liesche J, Fang H, Chen S (2017) A novel and efficient bioprocess from steam exploded corn stover to ethanol in the context of on-site cellulase production. Energy 123:499–510. https://doi.org/10.1016/j.energy.2017.02.041
Qi W, Chen C-L, Wang J-Y (2011) Reducing sugar-producing bacteria from guts of Tenebrio molitor Linnaeus (Yellow mealworm) for lignocellulosic waste minimization. Microbes Environ 26(4):354–359. https://doi.org/10.1264/jsme2.me11129
Zuo S, Niu D, Zheng M, Jiang D, Tian P, Li R, Xu C (2018) Effect of Irpex lacteus, Pleurotus ostreatus and Pleurotus cystidiosus pretreatment of corn stover on its improvement of the in vitro rumen fermentation. J Sci Food Agric 98:4287–4295. https://doi.org/10.1002/jsfa.8951
Premalatha M, Abbasi T, Abbasi T, Abbasi SA (2011) Energy-efficient food production to reduce global warming and ecodegradation: the use of edible insects. Renew Sust Energ Rev 15(9):4357–4360. https://doi.org/10.1016/j.rser.2011.07.115
US Department of Agriculture (2018) Production of soybean meal worldwide from 2013/14 to 2017/18, by country (in million metric tons). In: Statista. https://www.statista.com/statistics/612537/soybeanmeal-production-worldwide-by-country/. Accessed 23 Dec 2017
Xu J, Zhao Q, Qu Y, Ye F (2015) Antioxidant activity and anti-exercise-fatigue effect of highly denatured soybean meal hydrolysate prepared using neutrase. J Food Sci Technol 52(4):1982–1992. https://doi.org/10.1007/s13197-013-1220-7
Tian C, Wang J (2012) Analysis of the development status and trend of Chinese liquor industry. North Econ 1:108–109
Yang T, Rao Z, Zhang X, Xu M, Xu Z, Yang S-T (2015) Economic conversion of spirit-based distillers’ grain to 2, 3-butanediol by Bacillus amyloliquefaciens. Process Biochem 50(1):20–23. https://doi.org/10.1016/j.procbio.2014.11.006
Focus Technology Co. L (2018) Animal feed prices. https://www.made-in-china.com/products-search/hot-china-products/Soybean_Meal.html. Accessed 06/29 2018
Morales-Ramos J, Rojas M, Shapiro-Ilan D, Tedders W (2010) Developmental plasticity in Tenebrio molitor (Coleoptera: Tenebrionidae): analysis of instar variation in number and development time under different diets. J Entomol Sci 45(2):75–90. https://doi.org/10.18474/0749-8004-45.2.75
Yang Y, Yang J, Wu W-M, Zhao J, Song Y, Gao L, Yang R, Jiang L (2015) Biodegradation and mineralization of polystyrene by plastic-eating mealworms: Part 1. Chemical and physical characterization and isotopic tests. Environ Sci Technol 49(20):12080–12086. https://doi.org/10.1021/acs.est.5b02661
Ramos-Elorduy J, Gonzalez EA, Hernandez AR, Pino JM (2002) Use of Tenebrio molitor (Coleoptera: Tenebrionidae) to recycle organic wastes and as feed for broiler chickens. J Econ Entomol 95(1):214–220. https://doi.org/10.1603/0022-0493-95.1.214
Li L, Zhao Z, Liu H (2013) Feasibility of feeding yellow mealworm (Tenebrio molitor L.) in bioregenerative life support systems as a source of animal protein for humans. AcAau 92(1):103–109. https://doi.org/10.1016/j.actaastro.2012.03.012
Alves AV, Sanjinez-Argandona EJ, Linzmeier AM, Cardoso CAL, Macedo MLR (2016) Food value of mealworm grown on Acrocomia aculeata pulp flour. PLoS One 11(3):e0151275. https://doi.org/10.1371/journal.pone.0151275
Li M, Marek SM, Peng J, Liu Z, Wilkins (2018) Effect of moisture content and inoculum size on cell wall composition and ethanol yield from switchgrass after solid-state Pleurotus ostreatus treatment. Trans ASABE 61(6):1997–2006. https://doi.org/10.13031/trans.12981
Henry KM (1965) A comparison of biological methods with rats for determining the nutritive value of proteins. Br J Nutr 19(1):125–135. https://doi.org/10.1079/bjn19650012
AOAC (1990) Protein (crude) in animal feed: combustion method. (990.03). AOAC International, Arlington, VA, USA
Thiex NJ, Anderson S, Gildemeister B (2003) Crude fat, hexanes extraction, in feed, cereal grain, and forage (Randall/soxtec/submersion method): collaborative study. J AOAC Int 86(5):899–908
Thiex N, Novotny L, Crawford A (2012) Determination of ash in animal feed: AOAC official method 942.05 revisited. J AOAC Int 95(5):1392–1397. https://doi.org/10.5740/jaoacint.12-129
Liu K-L, Zheng J-B, Chen F-S (2017) Relationships between degree of milling and loss of Vitamin B, minerals, and change in amino acid composition of brown rice. LWT-Food Sci Technol 82(Supplement C):429–436. https://doi.org/10.1016/j.lwt.2017.04.067
Oser B (1951) Method for integrating essential ammo acid content in the nutritional evaluation of protein. J Am Diet Assoc 27:396–402
FAO/WHO/UNU (2007) Protein and amino acid requirements in human nutrition, vol 935. Report of a joint WHO/FAO/UNU Expert Consultation, vol 35. World Health Organization, Geneva
Paquot C, Hautfenne A (1987) Standard methods for the analysis of oils, fats and derivatives, vol 73. Blackwell Scientific London, London. https://doi.org/10.1515/iupac.53.0020
Peng D, Bi Y, Ren X, Yang G, Sun S, Wang X (2015) Detection and quantification of adulteration of sesame oils with vegetable oils using gas chromatography and multivariate data analysis. Food Chem 188:415–421. https://doi.org/10.1016/j.foodchem.2015.05.001
Hall FG, Jones OG, O’Haire ME, Liceaga AM (2017) Functional properties of tropical banded cricket (Gryllodes sigillatus) protein hydrolysates. Food Chem 224:414–422. https://doi.org/10.1016/j.foodchem.2016.11.138
Yi H-Y, Chowdhury M, Huang Y-D, Yu X-Q (2014) Insect antimicrobial peptides and their applications. Appl Microbiol Biotechnol 98(13):5807–5822. https://doi.org/10.1007/s00253-014-5792-6
Muller A, Wolf D, Gutzeit HO (2017) The black soldier fly, Hermetia illucens—a promising source for sustainable production of proteins, lipids and bioactive substances. Zeitschrift fur Naturforschung C 72(9–10):351–363. https://doi.org/10.1515/znc-2017-0030
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. Compr Rev Food Sci Food Saf 12(3):296–313
Kaya M, Baran T, Erdogan S, Mentes A, Asan Ozusaglam M, Cakmak YS (2014) Physicochemical comparison of chitin and chitosan obtained from larvae and adult Colorado potato beetle (Leptinotarsa decemlineata). Mater Sci Eng C 45:72–81. https://doi.org/10.1016/j.msec.2014.09.004
Wang X, Zheng X, Li X, Yao J, Jiang S, Zhang M (2010) Study on the biological characters of Tenebrio molitor L.[J]. Chin Agri Sci Bull 8:051
Bjorge JD, Overgaard J, Malte H, Gianotten N, Heckmann L-H (2018) Role of temperature on growth and metabolic rate in the tenebrionid beetles Alphitobius diaperinus and Tenebrio molitor. J Insect Physiol 107:89–96. https://doi.org/10.1016/j.jinsphys.2018.02.010
Fraenkel G (1950) The nutrition of the mealworm, Tenebrio molitor L. (Tenebrionidae, Coleoptera). Physiol Zool 23(2):92–108
House H (1965) Effects of low levels of the nutrient content of a food and of nutrient imbalance on the feeding and the nutrition of a phytophagous larva, Celerio euphorbiae (Linnaeus)(Lepidoptera: Sphingidae). Can Entomol 97(1):62–68
Morales-Ramos JA, Rojas MG, Shapiro-llan DI, Tedders WL (2013) Use of nutrient self-selection as a diet refining tool in Tenebrio molitor (Coleoptera: Tenebrionidae). J Entomol Sci 48(3):206–221. https://doi.org/10.18474/0749-8004-48.3.206
Gleadow RM, Woodrow IE (2002) Mini-review: constraints on effectiveness of cyanogenic glycosides in herbivore defense. J Chem Ecol 28(7):1301–1313
Rehman KU, Cai M, Xiao X, Zheng L, Wang H, Soomro AA, Zhou Y, Li W, Yu Z, Zhang J (2017) Cellulose decomposition and larval biomass production from the co-digestion of dairy manure and chicken manure by mini-livestock (Hermetia illucens L.). J Environ Manage 196(Supplement C):458–465. https://doi.org/10.1016/j.jenvman.2017.03.047
Varelas V, Langton M (2017) Forest biomass waste as a potential innovative source for rearing edible insects for food and feed—a review. Innov Food Sci Emerg Technol 41(Supplement C):193–205. https://doi.org/10.1016/j.ifset.2017.03.007
Fogang Mba AR, Kansci G, Viau M, Hafnaoui N, Meynier A, Demmano G, Genot C (2017) Lipid and amino acid profiles support the potential of Rhynchophorus phoenicis larvae for human nutrition. J Food Compost Anal 60(Supplement C):64–73. https://doi.org/10.1016/j.jfca.2017.03.016
Chapman RF (1998) The insects: structure and function, 4th edn. Cambridge University Press, Cambridge
Nielsen AS (2016) Screening of alternative feed substrates for production of Tenebrio molitor larvae. Aarhus University, Denmark
Paul A, Frederich M, Megido RC, Alabi T, Malik P, Uyttenbroeck R, Francis F, Blecker C, Haubruge E, Lognay G, Danthine S (2017) Insect fatty acids: A comparison of lipids from three Orthopterans and Tenebrio molitor L. larvae. J Asia-Pacif Entomol 20(2):337–340. https://doi.org/10.1016/j.aspen.2017.02.001
Ortiz J, Romero N, Robert P, Araya J, Lopez-Hernandez J, Bozzo C, Navarrete E, Osorio A, Rios A (2006) Dietary fiber, amino acid, fatty acid and tocopherol contents of the edible seaweeds Ulva lactuca and Durvillaea antarctica. Food Chem 99(1):98–104. https://doi.org/10.1016/j.foodchem.2005.07.027
Burkwall M Jr, Glass R (1965) The fatty acids of wheat and its milled products. Cereal Chem 42:236–246
Bendova O, Richter V, Janderova B, Hausler J (1991) Identification of industrial yeast strains of Saccharomyces cerevisiae by fatty acid profiles. Appl Microbiol Biotechnol 35(6):810–812. https://doi.org/10.1007/bf00169900
Barroso FG, Sanchez-Muros M-J, Segura M, Morote E, Torres A, Ramos R, Guil J-L (2017) Insects as food: enrichment of larvae of Hermetia illucens with omega 3 fatty acids by means of dietary modifications. J Food Compost Anal 62:8–13. https://doi.org/10.1016/j.jfca.2017.04.008
Dreassi E, Cito A, Zanfini A, Materozzi L, Botta M, Francardi V (2017) Dietary fatty acids influence the growth and fatty acid composition of the yellow mealworm Tenebrio molitor (Coleoptera: Tenebrionidae) lipids. Food Foodways 52(3):285–294. https://doi.org/10.1007/s11745-016-4220-3
Acknowledgements
This work was supported by the National Key R&D Program of China (Grant No. 2016YFD0400800) and National Science Foundation of China (Grant No. 31470090). The authors would like to thank Dr. Divya Ramchandran and Mr. Piyush Pandey at the University of Nebraska-Lincoln for proofreading the manuscript.
Author information
Authors and Affiliations
Corresponding authors
Ethics declarations
Conflict of interest
The authors declare that they have no conflict of interest.
Compliance with ethics requirements
This article does not contain any studies with human or animal subjects.
Additional information
Publisher's Note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Rights and permissions
About this article
Cite this article
Zhang, X., Tang, H., Chen, G. et al. Growth performance and nutritional profile of mealworms reared on corn stover, soybean meal, and distillers’ grains. Eur Food Res Technol 245, 2631–2640 (2019). https://doi.org/10.1007/s00217-019-03336-7
Received:
Revised:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s00217-019-03336-7