Abstract
Among edible insects, mealworms have attracted a lot of scientific and commercial attention as a nutrient source in food and feed during the last decade. However, the main focus has been on the yellow mealworm, Tenebrio molitor, which undisputedly possesses numerous advantages that render it ideal for mass production. Apart from the yellow mealworm though, other mealworm species have great potential for food and feed applications. The lesser mealworm and the superworm are two species that, although less studied, show promise and could gain their share of the edible insect market in the near future. The present publication aims to put the main edible mealworm species under the spotlight and give a brief overview of their potential as food and feed source.
1 Introduction
Mealworms (Coleoptera: Tenebrionidae), alternatively known as ‘darkling beetles’, owe their common name to their nocturnal behaviour and their habit of living in dark places (e.g. ‘Tenebrio’: Latin for ‘lover of darkness’). Because of this tendency to avoid light, mealworms were for decades considered secondary stored-product insect pests, usually found in silos and warehouses, infecting dry durable commodities (e.g. meals, hence the origin of their other common name) (Hagstrum and Subramanyam; 2009; Hagstrum et al., 2013). In a rare moment of publicity, mealworms left darkness for a while in order to travel, in September 1968, with an unmanned spacecraft to the moon and back, and so became one of the first animal species to fly around the moon (NASA, 2004). Afterwards, however, they returned once more to their dark habitats and their rather undignified role as secondary storage insects.
It was only after the release of a pioneering FAO publication (Van Huis, 2013), and a legendary conference ‘Insects to Feed the World’ (14-17 May 2014) in the Netherlands, which set the stage for the use of insects as food and feed, that mealworms started crawling out of their dark niches into the limelight, and featuring in the news. Since then, mealworms have attracted extensive research and commercial interest, as they possess a number of desirable traits for mass production as a nutrient source (Berezina, 2017). Among mealworms though, the yellow mealworm, Tenebrio molitor L., has been the ‘superstar’ of the tenebrionids, attracting the largest share of interest from the scientific community (Figure 1). Together with the black soldier fly, Hermetia illucens (L.) (Diptera: Stratiomyidae), which constitutes the ‘golden bowl’ of the insect sector, the yellow mealworms are the most studied edible insect species (Rumbos and Athanassiou, 2021a). This scientific interest has also been translated into a substantial commercial production, as the yellow mealworm possesses a big share of the edible insect market (Pippinato et al., 2020; Meticulous Market Research, 2022). And this not undeserved. Tenebrio molitor is easy to breed and rear, with no excessive requirements in handling and manipulation, and has a high reproduction rate and relatively rapid larval growth, traits that favour commercialisation (Berezina, 2017). Moreover, T. molitor larvae are highly nutritious, as they are rich in protein (45-68%) and fat (15-43%) (Rumbos et al., 2019 and references therein), but also vitamins and minerals (Oonincx and Finke, 2020). Moreover, they are efficient feed converters (Van Broekhoven et al., 2015), which means they can be reared using a variety of organic side-streams and by-products, adding extra sustainability credits to their production (Mancini et al., 2019; Rumbos et al., 2021a,b; Silva et al., 2021; Van Peer et al., 2021).
Number of published articles per year indexed by Google Scholar matching the search queries ‘Tenebrio molitor’, ‘Alphitobius diaperinus’, ‘Zophobas morio’ and ‘edible insect’, shown per year of publication (2010-2022) (Date of Google Scholar search: 27 September 2023).
Citation: Journal of Insects as Food and Feed 9, 11 (2023) ; 10.1163/23524588-230912ED
Numerous studies have also shown the suitability of T. molitor larvae as feed for several livestock animal species (Hong et al., 2020), e.g. poultry (Bovera et al., 2016; Biasato et al., 2018), pigs (Jin et al., 2016; Yoo et al., 2019), and farmed fish (Gasco et al., 2016; Piccolo et al., 2017; Iaconisi et al., 2018; Ido et al., 2019; Li et al., 2022; Mente et al., 2022). Additionally, recent works have also demonstrated the exploitation potential of T. molitor larvae in food for human consumption, in order to improve the nutritional and functional properties of food products (Zhao et al., 2016; Wendin et al., 2019, 2021; Djouadi et al., 2022). These advantages have led to the authorisation of T. molitor larvae for several food and feed applications in the EU, from the approval of their use as ingredients in aquafeeds back in 2017 (EU, 2017), a milestone in the exploitation of T. molitor as feed, to their authorisation in 2021 for poultry and swine diets (EU, 2021). Regarding food, T. molitor dried larvae and meal acquired the first EU-wide approval from the European Food Safety Authority (EFSA) for insect-derived food products, which was a breakthrough for the inclusion of insects in novel foods (EFSA, 2021). Apart from its usage in the food and feed sector, T. molitor can also be exploited in a number of industrial and technological applications, e.g. of the cosmetic (Kim et al., 2018; Verheyen et al., 2023) or the pharmaceutical industry (Song et al., 2018; Errico et al., 2021). Totally aligned with the circular economy and zero-waste concept, frass, the waste stream of T. molitor production, has been identified as an efficient soil fertiliser, enhancing plant growth and improving soil properties (Poveda et al., 2019; Houben et al., 2020). Finally, it has been shown recently that T. molitor and their gut microbes also have the ability to biodegrade several plastic types, such as polyethylene and polystyrene foam, introducing new prospects for the implementation of sustainable plastic waste management strategies (Brandon et al., 2018; Bulak et al., 2021; Sangiorgio et al., 2021; Wang and Tang, 2022). All the above explain the tremendous interest in the yellow mealworm. However, does the potential for exploitation refer only to the yellow mealworm?
2 Lesser but not least
One of the mealworm species that is considered suitable for food and feed applications and has also attracted research interest, although considerably less compared to T. molitor, is the lesser mealworm, Alphitobius diaperinus (Panzer) (Figure 1). Originally a common insect pest of commercial poultry farms (Axtell and Arends, 1990; Crippen and Poole, 2012; Sammarco et al., 2023), our perspective of this species changed after its inclusion in the list of EU-authorised insects for aquafeeds (EU, 2017). The approval of A. diaperinus for use in poultry and swine diets in 2021 (EU, 2021) and its recent authorisation as a novel food (EU, 2023) are expected to further boost research on this species for food and feed applications. Alphitobius diaperinus larvae have a valuable nutrient profile, with a high crude protein content (58-65%) and an amino acid composition similar to several nutritious foods, e.g. milk, meat or soybean protein; moreover, they are also rich in lipids (13-29%), minerals and other micronutrients (Yi et al., 2013; Churchward-Venne et al., 2017; Rumbos et al., 2019 and references therein; Kurečka et al., 2021). Despite its high nutrient value, studies for the replacement of traditional feedstocks, e.g. fishmeal, soybean meal, etc., in the diets of farmed livestock animals and fish are still limited. Apart from an older study with broilers chicks (Despins and Axtell, 1995), it was only recently that the results of feeding trials with A. diaperinus-based diets for fish (Gasco et al., 2022), pigs (Müller Richli et al., 2023), as well as ruminants (Renna et al., 2022; Toral et al., 2022) were published. The same goes for the exploitation of A. diaperinus for food applications, which has only recently started being investigated more intensively (Roncolini et al., 2020; Hermans et al., 2021).
3 Superworms for super foods and feeds
One mealworm species that is also promising as a nutrient source is the superworm, Zophobas morio (F.), as it has several desirable traits for food and feed applications. Briefly, Z. morio larvae are big in size (as suggested by their common name), and rich in protein (39-54%), lipids (35-44%) and other micronutrients (Rumbos and Athanassiou, 2021b and references therein). Despite its potential for inclusion in food and feed products, Z. morio has so far been largely overlooked by researchers (Figure 1) and commercial insect-producing companies. There are several possible reasons for this, e.g. the lack of official authorisation for food and feed in many parts of the world (incl. the EU), or technical production issues that have to be thoroughly clarified, such as the inability of Z. morio larvae to pupate in crowded conditions (Tschinkel and Willson, 1971) or their cannibalistic behaviour, especially where there is inadequate moisture (Ichikawa and Kurauchi, 2009). This suggests a need for optimisation of the technologies required for its mass production that will better permit the industrialisation of the production processes and positively impact its commercial production efficiency. Several studies have investigated the effect of the dietary inclusion of Z. morio meal in aquafeeds (Fontes et al., 2019; Alves et al., 2020; Mikołajczak et al., 2020; Henry et al., 2022), poultry (Kierończyk et al., 2018; Benzertiha et al., 2019, 2020; Józefiak et al., 2020) and pig diets (Liu et al., 2020), providing evidence for its suitability for the partial replacement of traditional feedstocks. Along the same lines, recent studies have also started to explore the potential of Z. morio for food applications (Scholliers et al., 2019, 2020a,b).
4 Closing remarks
There is no doubt that mealworms can play a key role in the current transition to more sustainable, efficient and environmentally friendly food and feed systems through insect inclusion in human and animal diets. The yellow mealworm has so far been one of the best ambassadors in this new era for edible insects. However, other mealworm species, such as the lesser mealworm and the superworm, also show promise as nutrient sources and should be further and more intensively investigated in this direction. Moreover, the mealworm edible species range could be further expanded in the future to include other related species. The dark or mini mealworm, Tenebrio obscurus (F.), which has also recently been shown to be able to biodegrade polystyrene (Peng et al., 2019), or the black fungus beetle, Alphitobius laevigatus (F.), which is already used as feed for house pets, e.g. reptiles, amphibians (Marien et al., 2022; Żuk-Gołaszewska et al., 2022), could be notable mealworm candidates for future research and subsequent commercial exploitation as nutrient sources. Only the future will tell, but it appears that the use of mealworms as food and feed is only just beginning!
Corresponding author; e-mail: crumbos@uth.gr
References
Alves, A.P.D.C., Paulino, R.R., Pereira, R.T., Costa, D.V.D. and Rosa, P.V., 2020. Nile tilapia fed insect meal: growth and innate immune response in different times under lipopolysaccharide challenge. Aquaculture Research 52: 529-540. https://doi.org/10.1111/are.14911
Axtell, R.C. and Arends, J.J., 1990. Ecology and management of arthropod pests of poultry. Annual Review of Entomology 35: 101-126. https://doi.org/10.1146/annurev.en.35.010190.000533
Benzertiha, A., Kierończyk, B., Rawski, M., Józefiak, A., Kozłowski, K., Jankowski, J. and Józefiak, D., 2019. Tenebrio molitor and Zophobas morio full-fat meals in broiler chicken diets: effects on nutrients digestibility, digestive enzyme activities, and cecal microbiome. Animals 12: 1128. https://doi.org/10.3390/ani9121128
Benzertiha, A., Kierończyk, B., Kołodziejski, P., Pruszyńska-Oszmałek, E., Rawski, M., Józefiak, D. and Józefiak, A., 2020. Tenebrio molitor and Zophobas morio full-fat meals as functional feed additives affect broiler chickens’ growth performance and immune system traits. Poultry Science 99: 196-206. https://doi.org/10.3382/ps/pez450
Berezina, N., 2017. Mealworms, promising beetles for the insect industry. In: Van Huis, A. and Tomberlin, J.K. (eds.) Insects as food and feed: from production to consumption. Wageningen Academic Publishers, Wageningen, The Netherlands, pp. 259-269. https://doi.org/10.3920/978-90-8686-849-0
Biasato, I., Gasco, L., De Marco, M., Renna, M., Rotolo, L., Dabbou, S., Capucchio, M.T., Biasibetti, E., Tarantola, M., Sterpone, L., Cavallarin, L., Gai, F., Pozzo, L., Bergagna, S., Dezzutto, D., Zoccarato, I. and Schiavone, A., 2018. Yellow mealworm larvae (Tenebrio molitor) inclusion in diets for male broiler chickens: effects on growth performance, gut morphology, and histological findings. Poultry Science 97: 540-548. http://dx.doi.org/10.3382/ps/pex308
Bovera, F., Loponte, R., Marono, S., Piccolo, G., Parisi, G., Iaconisi, V., Gasco, L. and Nizza, A., 2016. Use of Tenebrio molitor larvae meal as protein source in broiler diet: effect on growth performance, nutrient digestibility, and carcass and meat traits. Journal of Animal Science 94: 639-647. http://dx.doi.org/10.2527/jas2015-9201
Brandon, A.M., Gao, S.-H., Tian, R., Ning, D., Yang, S.-S., Zhou, J., Wu, W.-M. and Criddle, C.S., 2018. Biodegradation of polyethylene and plastic mixtures in mealworms (larvae of Tenebrio molitor) and effects on the gut microbiome. Environmental Science and Technology 52: 6526-6533. https://doi.org/10.1021/acs.est.8b02301
Bulak, P., Proc, K., Pytlak, A., Puszka, A., Gawdzik, B. and Bieganowski, A., 2021. Biodegradation of different types of plastics by Tenebrio molitor insect. Polymers 13: 3508. https://doi.org/10.3390/polym13203508
Churchward-Venne, T.A., Pinckaers, P.J.M., van Loon, J.J.A. and van Loon, L.J.C., 2017. Consideration of insects as a source of dietary protein for human consumption. Nutrition Reviews 75: 1035-1045. https://doi.org/10.1093/nutrit/nux057
Crippen, T.L. and Poole, T.L., 2012. Lesser mealworms on poultry farms: a potential arena for the dissemination of pathogen and antimicrobial resistance. In: Callaway, T.R. and Edrington, T.S. (eds.) On-farm strategies to control foodborne pathogens, pp. 233-272. Nova Science Publishers Inc., New York, NY, USA.
Despins, J.L. and Axtell, R.C., 1995. Feeding behavior and growth of broiler chicks fed larvae of the darkling beetle, Alphitobius diaperinus. Poultry Science 74: 331-336. https://doi.org/10.3382/ps.0740331
Djouadi, A., Sales, J.R., Carvalho, M.O. and Raymundo, A., 2022. Development of healthy protein-rich crackers using Tenebrio molitor flour. Foods 11: 702. https://doi.org/10.3390/foods11050702
Errico, S., Spagnoletta, A., Verardi, A., Moliterni, S., Dimatteo, S. and Sangiorgio, P., 2021. Tenebrio molitor as a source of interesting natural compounds, their recovery processes, biological effects, and safety aspects. Comprehensive Reviews in Food Science and Food Safety 21: 148-197. https://doi.org/10.1111/1541-4337.12863
EU, 2017. Commission regulation 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. Official Journal of the European Union 138: 92-116. Available online: https://eur-lex.europa.eu/legal-content/EN/TXT/PDF/?uri=CELEX:32017R0893&from=EN (accessed September 27, 2023).
EU, 2021. Commission regulation (EU) 2021/1372 of 17 August 2021 amending annex IV to regulation (EC) No 999/2001 of the European Parliament and of the council as regards the prohibition to feed non-ruminant farmed animals, other than fur animals, with protein derived from animals. Official Journal of the European Union 295: 1-17. Available online: https://eur-lex.europa.eu/legal-content/EN/TXT/PDF/?uri=CELEX:32021R1372 (accessed September 27, 2023).
EU, 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. Official Journal of the European Union 5: 10-15. (accessed September 27, 2023).
European Food Safety Authority (EFSA) NDA Panel (EFSA Panel on Nutrition, Novel Foods and Food Allergens), Turck, D., Castenmiller, J., De Henauw, S., Hirsch-Ernst, K.I., Kearney, J., Maciuk, A., Mangelsdorf, I., McArdle, H.J., Naska, A., Pelaez, C., Pentieva, K., Siani, A., Thies, F., Tsabouri, S., Vinceti, M., Cubadda, F., Frenzel, T., Heinonen, M., Marchelli, R., Neuhäuser-Berthold, M., Poulsen, M., Prieto Maradona, M., Schlatter, J.R., van Loveren, H., Ververis, E. and Knutsen, H.K., 2021. Scientific opinion on the safety of dried yellow mealworm (Tenebrio molitor larva) as a novel food pursuant to regulation (EU) 2015/2283. EFSA Journal 19: 6343. Available online: https://doi.org/10.2903/j.efsa.2021.6343 (accessed September 27, 2023).
Fontes, T.V., de Oliveira, K.R.B., Gomes Almeida, I.L., Maria Orlando, T., Rodrigues, P.B., Costa, D.V. and Rosa, P.V., 2019. Digestibility of insect meals for Nile tilapia fingerlings. Animals 9: 181. https://doi.org/10.3390/ani9040181
Gasco, L., Henry, M., Piccolo, G., Marono, S., Gai, F., Renna, M., Lussiana, C., Antonopoulou, E., Mola, P. and Chatzifotis, S., 2016. Tenebrio molitor meal in diets for European sea bass (Dicentrarchus labrax L.) juveniles: growth performance, whole body composition and in vivo apparent digestibility. Animal Feed Science and Technology 220: 34-45. http://dx.doi.org/10.1016/j.anifeedsci.2016.07.003
Gasco, L., Caimi, C., Trocino, A., Lussiana, C., Oddon, S.B., Malfatto, V., Anedda, R., Serra, G., Biasato, I., Schiavone, A., Gai, F. and Renna, M., 2022. Digestibility of defatted insect meals for rainbow trout aquafeeds. Journal of Insects as Food and Feed 8: 1385-1399. https://doi.org/10.3920/JIFF2021.0160
Hagstrum, D.W. and Subramanyam, B., 2009. Stored-product insect resource. AACC International Inc., St. Paul, MN, USA.
Hagstrum, D.W., Klejdysz, T., Subramanyam, B. and Nawrot, J., 2013. Atlas of stored-product insects and mites. AACC International Inc., St. Paul, MN.
Henry, M.A., Golomazou, E., Asimaki, A., Psofakis, P., Fountoulaki, E., Mente, E., Rumbos, C.I., Athanassiou, C.G. and Karapanagiotidis, I.T., 2022. Partial dietary fishmeal replacement with full-fat or defatted superworm (Zophobas morio) larvae meals modulates the innate immune system of gilthead seabream, Sparus aurata. Aquaculture Reports 27: 101347. https://doi.org/10.1016/j.aqrep.2022.101347
Hermans, W.J.H., Senden, J.M., Churchward-Venne, T.A., Paulussen, K.J.M., Fuchs, C.J., Smeets, J.S.J., van Loon, J.J.A., Verdijk, L.B. and van Loon, L.J.C., 2021. Insects are a viable protein source for human consumption: from insect protein digestion to postprandial muscle protein synthesis in vivo in humans: a double-blind randomized trial. The American Journal of Clinical Nutrition 114: 934-944.
Hong, J., Han, T. and Kim, Y.Y., 2020. Mealworm (Tenebrio molitor larvae) as an alternative protein source for monogastric animal: a review. Animals 10: 2068. https://doi.org/10.3390/ani10112068
Houben, D., Daoulas, G., Faucon, M.-P. and Dulaurent, A.-M., 2020. Potential use of mealworm frass as a fertilizer: impact on crop growth and soil properties. Scientific Reports 10: 4659. https://doi.org/10.1038/s41598-020-61765-x
Iaconisi, V., Bonelli, A., Pupino, R., Gai, F. and Parisi, G., 2018. Mealworm as dietary protein source for rainbow trout: body and fillet quality traits. Aquaculture 484: 197-204. https://doi.org/10.1016/j.aquaculture.2017.11.034
Ichikawa, T. and Kurauchi, T., 2009. Larval cannibalism and pupal defense against cannibalism in two species of tenebrionid beetles. Zoological Science 26: 525-529. https://doi.org/10.2108/zsj.26.525
Ido, A., Hashizume, A., Ohta, T., Takahashi, T., Miura, C. and Miura, T., 2019. Replacement of fish meal by defatted yellow mealworm (Tenebrio molitor) larvae in diet improves growth performance and disease resistance in red seabream (Pargus major). Animals 9: 100. http://dx.doi.org/10.3390/ani9030100
Jin, X.H., Heo, P.S., Hong, J.S., Kim, N.J. and Kim, Y.Y., 2016. Supplementation of dried mealworm (Tenebrio molitor larva) on growth performance, nutrient digestibility and blood profiles in weaning pigs. Asian Australasian Journal of Animal Science 29: 979-986. http://dx.doi.org/10.5713/ajas.15.0535
Józefiak, A., Benzertiha, A., Kierończyk, B., Łukomska, A., Wesołowska, I. and Rawski, M., 2020. Improvement of cecal commensal microbiome following the insect additive into chicken diet. Animals 10: 577. https://doi.org/10.3390/ani10040577
Kierończyk, B., Rawski, M., Józefiak, A., Mazurkiewicz, J., Świątkiewicz, S., Siwek, M., Bednarczyk, M., Szumacher-Strabel, M., Cieślak, A., Benzertiha, A. and Józefiak, D., 2018. Effects of replacing soybean oil with selected insect fats on broilers. Animal Feed Science and Technology 240: 170-183. https://doi.org/10.1016/j.anifeedsci.2018.04.002
Kim, J.J., Kim, K.S. and Yu, B.J., 2018. Optimization of antioxidant and skin-whitening compounds extraction condition from Tenebrio molitor larvae (mealworm). Molecules 23: 2340. http://dx.doi.org/10.3390/molecules23092340
Kurečka, M., Kulma, M., Petřı́čková, D., Plachý, V. and Kouřimská, L., 2021. Larvae and pupae of Alphitobius diaperinus as promising protein alternatives. European Food Research and Technology 247: 2527-2532. https://doi.org/10.1007/s00217-021-03807-w
Li, H., Hu, Z., Liu, S., Sun, J. and Ji, H., 2022. Influence of dietary soybean meal replacement with yellow mealworm (Tenebrio molitor) on growth performance, antioxidant capacity, skin color, and flesh quality of mirror carp (Cyprinus carpio var. specularis). Aquaculture 561: 738686 https://doi.org/10.1016/j.aquaculture.2022.738686
Liu, H., Tan, B., Kong, X., Li, J., Li, G., He, L., Bai, M. and Yin, Y., 2020. Dietary insect powder protein sources improve protein utilization by regulation on intestinal amino acid-chemosensing system. Animals 10: 1590. https://doi.org/10.3390/ani10091590
Mancini, S., Fratini, F., Turchi, B., Mattioli, S., Bosco, A.D., Tuccinardi, T., Nozic, S. and Paci, G., 2019. Former foodstuff products in Tenebrio molitor rearing: effects on growth, chemical composition, microbiological load, and antioxidant status. Animals 9: 484. https://doi.org/10.3390/ani9080484
Marien, A., Sedefoglu, H., Dubois, B., Maljean, J., Francis, F., Berben, G., Guillet, S., Morin, J.F., Fumière, O. and Debode, F., 2022. Detection of Alphitobius diaperinus by real-time polymerase chain reaction with a single-copy gene target. Frontiers in Veterinary Science 9: 718806. https://doi.org/10.3389/fvets.2022.718806
Mente, E., Bousdras, T., Feidantsis, K., Panteli, N., Mastoraki, M., Kormas, K.A., Chatzifotis, S., Piccolo, G., Gasco, L., Gai, F., Martin, S.A.M. and Antonopoulou, E., 2022. Tenebrio molitor larvae meal inclusion affects hepatic proteome and apoptosis and/or autophagy of three farmed fish species. Scientific Reports 12: 121. https://doi.org/10.1038/s41598-021-03306-8
Meticulous Market Research, 2022. Edible Insects Market by Product (Whole Insect, Insect Powder, Insect Meal, Insect Oil), Insect Type (Crickets, Black Soldier Fly, Mealworms), Application (Animal Feed, Protein Bar & Shakes, Bakery, Confectionery, Beverages), and Geography – Forecast to 2030. Available at: https://www.researchandmarkets.com/report/edible-insects
Mikołajczak, Z., Rawski, M., Mazurkiewicz, J., Kierończyk, B. and Józefiak, D., 2020. The effect of hydrolyzed insect meals in sea trout fingerling (Salmo trutta m. trutta) diets on growth performance, microbiota and biochemical blood parameters. Animals 10: 1031. https://doi.org/10.3390/ani10061031
Müller Richli, M., Weinlaender, F., Wallner, M., Pöllinger-Zierler, B., Kern, J. and Scheeder, M.R.L., 2023. Effect of feeding Alphitobius diaperinus meal on fattening performance and meat quality of growing-finishing pigs. Journal of Applied Animal Research 51: 204-211, https://doi.org/10.1080/09712119.2023.2176311
NASA (National Aeronautics and Space Administration), 2004. A brief history of animals in space. Available at: https://history.nasa.gov/animals.html
Oonincx, D.G.A.B. and Finke, M.D., 2020. Nutritional value of insects and ways to manipulate their composition. Journal of Insects as Food and Feed 7: 639-659. https://doi.org/10.3920/JIFF2020.0050
Peng, B.-Y., Su, Y., Chen, Z., Chen, J., Zhou, X., Benbow, M.E., Criddle, C.S., Wu, W.-M. and Zhang, Y., 2019. Biodegradation of polystyrene by dark (Tenebrio obscurus) and yellow (Tenebrio molitor) mealworms (Coleoptera: Tenebrionidae). Environmental Science and Technology 53: 5256-5265. https://doi.org/10.1021/acs.est.8b06963
Piccolo, G., Iaconisi, V., Marono, S., Gasco, L., Loponte, R., Nizza, S., Bovera, F. and Parisi, G., 2017. Effect of Tenebrio molitor larvae meal on growth performance, in vivo nutrients digestibility, somatic and marketable indexes of gilthead sea bream (Sparus aurata). Animal Feed Science and Technology 226: 12-20. http://dx.doi.org/10.1016/j.anifeedsci.2017.02.007
Pippinato, L., Gasco, L., Di Vita, G. and Mancuso, T., 2020. Current scenario in the European edible-insect industry: a preliminary study. Journal of Insect as Food and Feed 6: 371-381. https://doi.org/10.3920/JIFF2020.0008
Poveda, J., Jiménez-Gómez, A., Saati-Santamarı́a, Z., Usategui-Martı́n, R., Rivas, R. and Garcı́a-Fraile, P., 2019. Mealworm frass as a potential biofertilizer and abiotic stress tolerance-inductor in plants. Applied Soil Ecology 142: 110-122. https://doi.org/10.1016/j.apsoil.2019.04.016
Renna, M., Coppa, M., Lussiana, C., Le Morvan, A., Gasco, L. and Maxin, G., 2022. Full-fat insect meals in ruminant nutrition: in vitro rumen fermentation characteristics and lipid biohydrogenation. Journal of Animal Science and Biotechnology 13: 138. https://doi.org/10.1186/s40104-022-00792-2
Roncolini, A., Milanović, V., Aquilanti, L., Cardinali, F., Garofalo, C., Sabbatini, R., Clementi, F., Belleggia, L., Pasquini, M., Mozzon, M., Foligni, R., Trombetta, M.F., Haouet, M.N., Altissimi, M.S., Di Bella, S., Piersanti, A., Griffoni, F., Reale, A., Niro, S. and Osimani, A., 2020. Lesser mealworm (Alphitobius diaperinus) powder as a novel baking ingredient for manufacturing high-protein, mineral-dense snacks. Food Research International 131: 109031. https://doi.org/10.1016/j.foodres.2020.109031
Rumbos, C.I., Karapanagiotidis, I.T., Mente, E. and Athanassiou, C.G., 2019. The lesser mealworm Alphitobius diaperinus: a noxious pest or a promising nutrient source? Reviews in Aquaculture 11: 1418-1437. https://doi.org/10.1111/raq.12300
Rumbos, C.I. and Athanassiou, C.G.A., 2021a. ‘Insects as food and feed: if you can’t beat them, eat them!’ – to the magnificent seven and beyond. Journal on Insect Science 21: 9. https://doi.org/10.1093/jisesa/ieab019
Rumbos, C.I. and Athanassiou, C.G., 2021b. The giant mealworm, Zophobas morio: a “sleeping giant” in nutrient sources. Journal of Insect Science Journal of Insect Science 21: 13. https://doi.org/10.1093/jisesa/ieab014
Rumbos, C.I., Bliamplias, D., Gourgouta, M., Michail, V. and Athanassiou, C.G., 2021a. Rearing Tenebrio molitor and Alphitobius diaperinus larvae on seed cleaning process byproducts. Insects 12: 293. https://doi.org/10.3390/insects12040293
Rumbos, C.I., Oonincx, D.G.A.B., Karapanagiotidis, I.T., Vrontaki, M., Gourgouta, M., Asimaki, A., Mente, E. and Athanassiou, C.G., 2021b. Agricultural byproducts from Greece as feed for yellow mealworm larvae: circular economy at local level. Journal of Insects as Food and Feed 8: 9-22. https://doi.org/10.3920/JIFF2021.0044
Sammarco, B.C., Hinkle, N.C. and Crossley, M.S., 2023. Biology and management of lesser mealworm Alphitobius diaperinus (Coleoptera: Tenebrionidae) in broiler houses. Journal of Integrated Pest Management 14: 2. https://doi.org/10.1093/jipm/pmad003
Sangiorgio, P., Verardi, A., Dimatteo, S., Spagnoletta, A., Moliterni, S. and Errico, S., 2021. Tenebrio molitor in the circular economy: a novel approach for plastic valorisation and PHA biological recovery. Environmental Science and Pollution Research 28: 52689-52701. https://doi.org/10.1007/s11356-021-15944-6
Scholliers, J., Steen, L., Glorieux, S., Van de Walle, D., Dewettinck, K. and Fraeye, I., 2019. The effect of temperature on structure formation in three insect batters. Food Research International 122: 411-418. https://doi.org/10.1016/j.foodres.2019.04.033
Scholliers, J., Steen, L. and Fraeye, I., 2020a. Partial replacement of meat by superworm (Zophobas morio larvae) in cooked sausages: effect of heating temperature and insect: meat ratio on structure and physical stability. Innovative Food Science and Emerging Technologies 66: 102535. https://doi.org/10.1016/j.ifset.2020.102535
Scholliers, J., Steen, L. and Fraeye, I., 2020b. Structure and physical stability of hybrid model systems containing pork meat and superworm (Zophobas morio larvae): the influence of heating regime and insect: meat ratio. Innovative Food Science and Emerging Technologies 65: 102452. https://doi.org/10.1016/j.ifset.2020.102452
Silva, L.B., de Souza, R.G., da Silva, S.R., Feitosa, A.d.C., Lopes, E.C., Lima, S.B.P., Dourado, L.R.B. and Pavan, B.E., 2021. Development of Tenebrio molitor (Coleoptera: Tenebrionidae) on poultry litter-based diets: effect on chemical composition of larvae. Journal of Insect Science 21: 7. https://doi.org/10.1093/jisesa/ieaa145
Song, Y.-S., Kim, M.-W., Moon, C., Seo, D.-J., Han, Y.S., Jo, Y.H., Noh, M.Y., Park, Y.-K., Kim, S.-A., Kim, Y.W. and Jung, W.-J., 2018. Extraction of chitin and chitosan from larval exuvium and whole body of edible mealworm, Tenebrio molitor. Entomological Research 48: 227-233. https://doi.org/10.1111/1748-5967.12304
Toral, P.G., Hervás, G., González-Rosales, M.G., Mendoza, A.G., Robles-Jiménez, L.E. and Frutos, P., 2022. Insects as alternative feed for ruminants: comparison of protein evaluation methods. Journal of Animal Science and Biotechnology 13: 1-8. https://doi.org/10.1186/s40104-021-00671-2
Tschinkel, W.R. and Willson, C.D., 1971. Inhibition of pupation due to crowding in some tenebrionid beetles. Journal of Experimental Zoology 176: 137-145. https://doi.org/10.1002/jez.1401760203
Van Broekhoven, S., Oonincx, D.G.A.B., Van Huis, A. and van Loon, J.J.A., 2015. Growth performance and feed conversion efficiency of three edible mealworm species (Coleoptera: Tenebrionidae) on diets composed of organic by-products. Journal of Insect Physiology 73: 1-10. https://doi.org/10.1016/j.jinsphys.2014.12.005
Van Huis, A., Van Itterbeeck, J., Klunder, H., Mertens, E., Halloran, A., Muir, G. and Vantomme, P., 2013. Edible insects: future prospects for food and feed security. FAO forestry paper 171. Food and Agriculture Organization of the United Nations, Rome and Wageningen University and Research Centre, The Netherlands. Pp. 187. Available at: https://www.fao.org/3/i3253e/i3253e.pdf
Van Peer, M., Frooninckx, L., Coudron, C., Berrens, S., Álvarez, C., Deruytter, D., Verheyen, G. and Van Miert, S., 2021. Valorisation potential of using organic side streams as feed for Tenebrio molitor, Acheta domesticus and Locusta migratoria. Insects 12: 796. https://doi.org/10.3390/insects12090796
Verheyen, G.R., Meersman, F., Noyens, I., Goossens, S. and Van Miert, S., 2023. The application of mealworm (Tenebrio molitor) oil in cosmetic formulations. European Journal of Lipid Science and Technology 125: 2200193. https://doi.org/10.1002/ejlt.202200193
Wang, X. and Tang, T., 2022. Effects of polystyrene diet on the growth and development of Tenebrio molitor. Toxics 10: 608. https://doi.org/10.3390/toxics10100608
Wendin, K., Olsson, V. and Langton, M., 2019. Mealworms as food ingredient – sensory investigation of a model system. Foods 8: 319. https://doi.org/10.3390/foods8080319
Wendin, K., Berg, J., Jönsson, K.I., Andersson, P., Birch, K., Davidsson, F., Gerberich, J., Rask, S. and Langton, M., 2021. Introducing mealworm as an ingredient in crisps and patés – sensory characterization and consumer liking. Future Foods 4: 100082. https://doi.org/10.1016/j.fufo.2021.100082
Yi, L., Lakemond, C.M.M., Sagis, L.M.C., Eisner-Schadler, V., van Huis, A. and van Boekel, M.A.J.S., 2013. Extraction and characterisation of protein fractions from five insect species. Food Chemistry 141: 3341-3348. https://doi.org/10.1016/j.foodchem.2013.05.115
Yoo, J.S., Cho, K.H., Hong, J.S., Jang, H.S., Chung, Y.H., Kwon, G.T., Shin, D.G. and Kim, Y.Y., 2019. Nutrient ileal digestibility evaluation of dried mealworm (Tenebrio molitor) larvae compared to three animal protein by-products in growing pigs. Asian-Australasian Journal of Animal Science 32: 387-394. https://doi.org/10.5713/ajas.18.0647
Zhao, X., Vazquez-Gutiérrez, J.L., Johansson, D.P., Landberg, R. and Langton, M., 2016. Yellow mealworm protein for food purposes – extraction and functional properties. PLoS ONE 11: e0147791. https://doi.org/10.1371/journal.pone.0147791
Żuk-Gołaszewska, K., Gałęcki, R., Obremski, K., Smetana, S., Figiel, S. and Gołaszewski, J., 2022. Edible insect farming in the context of the EU regulations and marketing – an overview. Insects 13: 446. https://doi.org/10.3390/insects13050446
