Abstract
Larvae of the mealworm beetle Tenebrio molitor is commonly used as feed for pets and food for humans due to its rich nutrient contents. The beetle breeds prolifically and are reared in close proximity with their diet; known as substrates. However, the most commonly used substrate, wheat bran, is expensive making the rearing out of reach to many, especially in developing countries. This study evaluated the suitability of six other potential substrates; wheat flour, maize flour, Lucerne pellets, dog food, soya four and oats in comparison to wheat bran in order to explore a cost-effective alternative rearing substrate for mealworms. To achieve this, the mealworms were reared in a climate-controlled chamber and the total numbers, weight and the fecundity were determined for each substrate. Wheat bran and wheat flour produced the most mealworms, had the highest fecundity with wheat bran, Lucerne pellets an oat producing heavier worms than all other substrates. Maize flour, wheat flour and Lucerne, were found to be the most cost-effective alternative substrates for rearing mealworms with the cost per gram at 0.07, 0.05 and 0.04 US$ respectively. Both wheat flour and maize flour are easily accessible, have a long self-life thus ideal for both large-and small-scale production.
Graphical Abstract
Similar content being viewed by others
Avoid common mistakes on your manuscript.
Introduction
A growing human population projected to reach 9.8 billion by the year 2050; 11 billion in 2100 (UN 2017) makes the exploration and sustainable use of resources including food necessary. Attaining food security requires the provision and access to protein rich diets of which the current protein sources are most likely not able to cope with due to rising demands. Thus, making the quest for alternative, cheap and sustainable protein sources necessary. One such alternative protein source is from edible insects, which are easy to rear, rich in nutrients, have low ecological footprint and a high feed conversion efficiency (van Huis and Oonincx 2017). The use of insects as an alternative source of protein is common in Africa, Australia, Asia, South America and it is fast attracting interest in Europe and North America (Tucker 2013). Data from the Food and Agriculture Organization of the United Nations (FAO) indicates that over two billion people around the world incorporate edible insects into their diets (van Huis et al. 2013).
The larvae of the yellow mealworm beetle Tenebrio molitor L, belonging to the darkling beetles’ family Tenebrionidae are used as alternative animal protein sources for food and feed due to their nutritional value; ease of rearing, low ecological footprint and high feed conversion efficiency. In comparison to conventional meat such as beef and chicken, mealworms are rich in protein, fat, polyunsaturated fatty acids and are a good source of zinc, magnesium and calcium (Nowak et al. 2016; Payne et al. 2016; Grau et al. 2017). However, the nutritional value of mealworms varies between fresh (live) and dried larvae. Live mealworm larvae contains about 20% protein, 13% fat, and 62% moisture, whilst when dried the nutrient contents are enhanced with protein increasing to 53%, fat 28% and moisture decreasing to 5% (Abdalbasit et al. 2017). In addition, mealworms are sources of niacin, pyridoxine, riboflavin, vitamin B12, folate and all essential amino acids (Rumpold and Schlüter 2013; Nowak et al. 2016). Tenebrio molitor has a very low rearing requirement and can be reared on both small and large scales (Mancini et al. 2020) at a temperature of 25 °C and 27 °C. Rearing is often achieved by providing nesting and oviposition sites (usually a small container) and a substrate (diet). The beetle lays about 500 ovoid and elongated eggs that attaches to surfaces of containers or food source and hatches into a small (± 3 mm) white larvae in 4–19 days. In few days the larvae becomes yellow and form a hard chitinous exoskeleton (Siemianowska et al. 2013) and then passes through 9 to 20 instars. The last instar larvae which is used as human food weigh approximately 0.2 g and is 25–35 mm long (Aguilar-Miranda et al. 2002; Ghaly and Alkoaik 2009). The last instar larvae moult to produce a pale cream coloured pupa approximately 12–18 mm long, which develops into adult in six days. Mealworms are reared in a dense environment in close contact with their feed (substrate) (Mancini et al. 2020). The most commonly used substrate is wheat bran (Dreassi et al. 2017). However, wheat bran is expensive with a kg costing around US$ 1.05 (ZAR 15) making it unaffordable for smallholder farmers, community or low-income households seeking an alternative income supplement for conventional proteins sources or for use as animal feed.
For successful integration as alternative protein and nutrient sources, it is important that quality mealworms are produced using cheap and readily available substrates that can be integrated into current approaches, efforts and programs aimed at sustainable development (van Zyl and Malan 2015). As such, this study evaluated six readily available substrates for rearing mealworms with the aim of selecting the most cost-effective alternative to wheat bran.
Materials and methods
Mealworms
The starter colony of T. molitor adults were obtained from the rearing stock maintained at the Department of Zoology and Entomology University of Pretoria. This rearing colony has been ongoing for about seven years (since 2013) and is being restocked with new pairs quarterly in order to prevent inbreeding and maintain its genetic diversity. The colony was maintained in plastic boxes (43 cm × 28 cm × 13 cm), placed in a climate-controlled chamber, kept at a constant temperature of 25 ± 1 °C and a 0-hour light: 24-hour dark photoperiod on standard wheat bran as substrate.
Rearing substrates
Seven substrates were evaluated in this study. These include wheat flour (Supreme Foods Limited, South Africa), oats (Jungle oats Tiger Brands Limited South Africa), dog food pellets (EPOL Afrique Pet Foods, South Africa), Lucerne (Alfalfa) pellets (Midfeeds Limited South Africa), soya bean flour (Midfeeds Limited South Africa), maize flour (IWISA, Premier Foods, South Africa) and wheat bran (Supplementary Table S1).
Mealworm rearing, weights and fecundity on substrates
Two kilograms of each substrate was placed into clean and sterilised plastic rearing containers (68.4 × 38.4 × 20.9 cm, manufacturer: Plastilon Packaging, Pretoria, South Africa), spread out evenly, and ten grams (10 g) of fresh potato added to serve as a source of moisture. Thereafter, ten pairs of adult T. molitor (10 males and 10 females) were placed into each rearing container for three weeks (to allow for mating and oviposition), after which all the adult pairs were removed. Each substrate was replicated thrice making a total of 21 rearing containers.
After 45 days, the larvae of T. molitor hereafter ‘mealworms’ were removed by hand from each rearing container for the coarse substrates (Lucerne pellets) while for finer ones such as the flours a sieve with a mesh size of 3.00mm was used. Smaller individuals that passed through the sieve were handpicked.
The number of mealworms produced, and the fecundity (number of young produced per female) were then assessed for each substrate. Fecundity was determined by dividing the total number of individual mealworms produced per rearing box by the number of adult females used at the start of the experiment (F = Ni/Nf, where F is the fecundity, Ni is the number of individuals produced, and Nf is the number of females).
Total weights and the mean weight of each mealworm was determined by weighing on an Acculab ALC-801.2 Precision balance (Sartorius Group, USA). To determine the average weight of the individual mealworms per gram of substrate produced, the total weight was divided by the number of individuals produced for each rearing box (Average weight = Tw/Ni, where Tw is the total weight and Ni is the number of individuals produced for each rearing box).
The cost of mealworms per gram of substrate for each substrate was calculated by dividing the price per a kilogram of substrate (ZAR/kg) by average weight of the individual mealworms per kilogram of substrate produced (AW) (cost per gram = ZAR/kg / AW).
Statistical analyses
To test if there is a significant difference in the yield of mealworms and the price of the substrate, as well as to determine the most economical substrate to use, an ANOVA was performed using the weight and number of individuals as the dependent variable with substrates as grouping variables. Where means were significant, a Post Hoc analysis was conducted and means separated using Dunnett’s test for multiple comparison. To visualise the data, box and whisker plots were made to illustrate differences between the diets for all the different variables. All statistical analyses were carried out in R Studio version 1.2.5033 (RStudio Team 2020) and tests were deemed significant when p < 0.05.
Results
During the rearing, soya bean flour did not produce any individuals, whilst the dog pellets only produced one individual. Therefore, these substrates were deemed unsuitable for raising mealworms and removed from the experiment (Supplementary Figure S1 for the survival of mating pairs on each substrate). From the four alternative substrates, all measured variables; number of individuals produced (Fig. 1), total weight, weight of individuals and fecundity were different in comparison to wheat bran (ANOVA, multiple comparison, Wilks = 0.02, F = 8.53, df = 16, p < 0.05, Table 1).
Total weight of mealworms produced per substrate
The total weight of mealworms differs significantly between the five substrates (ANOVA, df = 4, F = 25.77, p < 0.05) with wheat bran producing mealworms that are on average 5 times heavier than other substrates (Fig. 2). Mealworms reared on wheat bran weighed an average total of 110.36 g while those reared on wheat flour, maize flour, Lucerne and oats weight an average between 28.81 g (oats) and 20.43 g (wheat flour) (Fig. 2).
Weights of individual mealworm per substrate
When comparing the mean weights of an individual mealworm produced per substrate, wheat bran, Lucerne and oats produced significantly heavier individuals (0.11 g, 0.10 g and 0.09 g respectively) than both the wheat and maize flour (0.02 and 0.05 g respectively (ANOVA, df = 4, F = 34.9, p < 0.05, Fig. 3).
Fecundity of females per substrate
Fecundity of adult beetles were different between all substrates (ANOVA, df = 4, F = 11.33, p < 0.05) with females reared on wheat bran producing more larvae (107 ± 5) followed by wheat flour (93 ± 5), maize flour (48 ± 5), Lucerne (26 ± 5) and oats (31 ± 5) (Fig. 4).
Cost per gram of mealworm produced
A comparison of the price per gram of mealworms produced (ZAR/US$/g) from each of the substrates is shown on Table 2. The price per gram of mealworms produced varied significantly among substrates (ANOVA, df = 4, F = 4.53, p < 0.05).
Discussion
Seven substrates for the rearing of T. molitor larvae (mealworms), a common insect used as food or feed, were evaluated. Of these, only wheat bran, wheat flour, maize flour, Lucerne and oats produced mealworms. No mealworms were produced on the soya flour substrate as all adults died within five days of initiating the experiment in all three replicates conducted. This was despite the fact that mating was observed between adults within the first few hours of being placed in the soya flour. The death of adults and the absence of egg laying could be due to the high protein content (49.3%) and low carbohydrates (18.6%) in soya flour (Farzana and Mohajan 2015). This can possibly be overcome by mixing or fortifying soya meal with another substrate that contains high carbohydrates as supplementing rearing substrates had been shown to improve both biomass and weights of mealworms (Deen et al. 2021).
More individual mealworms and fecund females were produced on wheat bran and wheat flour, with the latter producing heavier individuals. Thus, corroborating earlier findings by Rumbos et al. (2020) that wheat flours produced heavy mealworms. Although rearing mealworms on wheat bran supplemented with yeast has been shown to improve adult survival and increased number of larvae (Deen et al. 2021). This is expensive for small-scale farmers as such there is a need to explore economically viable substrates in order to facilitate their integration in current approaches, efforts and programs aimed at sustainable production of edible insects (van Zyl and Malan 2015). Dog food pellets did not also yield some mealworms and this could be attributed to its properties such as the presences of additives like oils, flavourings and or preservatives. In addition, dog food pellets are expensive costing twice as much as white flour and three times more than maize flour, thus making it not a good substrate for rearing mealworms.
Adult females of T. molitor were more fecund in wheat bran, wheat flour and maize flour due to the smaller grain size of these substrates, which makes it easier for both the larvae and adults to move in, lay eggs and feed in comparison to larger grained substrates like dog food pellets and Lucerne. Stored product pests are known to display preferences for oviposition substrates as seen in the larger grain borer Prostephanus truncatus which preferred maize on the cob than shelled maize (reviewed in Quellhorst et al. 2021) and, the cowpea weevil Callosobruchus maculatus which prefers to oviposit on waxed than non-waxed varieties (Poulami et al. 2016).
Larvae successfully hatched from five of the seven substrates within a week of removing the adults and 28 days from the introduction of adults to the substrate. Although wheat bran is more expensive in comparison to wheat flour, maize flour, Lucerne and oats, it remains the most cost-effective (Melis et al. 2019) substrate rearing mealworm out of those evaluated. However, we found wheat flour, maize flour, and Lucerne to offer the potential to serve as alternative substrates for subsistent and large-scale mealworm rearing in agreement to the quest to develop sustainable mass rearing (Egonyu et al. 2021; Niassy et al. 2022) valuable enterprise (Tanga et al. 2021) for edible insects towards attaining sustainable development in Africa. Although Lucerne is not as widely available as maize and wheat flour, it produced heavier mealworms. In addition, maize flour, and wheat flour have a long shelf life similar to wheat bran. The removal of the mealworms from both the maize and the wheat flour was also easier because the worms are visible and could be sieved or picked out. Fortifying both substrates with other nutrients could increase their suitability for mealworm productions.
Conclusion
The most cost-effective substrate remains the wheat bran however; wheat flour, Lucerne and maize flour were found to be potentially cost-effective and efficient alternatives for wheat bran. These substrates are cheap, easily accessible for both large-scale use as well as small-scale household farms and have long shelf life. Further research should be undertaken with the aim of increasing their efficiency or reducing the cost of using wheat bran by mixing these substrates together in different ratios with wheat bran. The nutrient contents, health and safety of mealworms raised on these substrates also need to be studied.
References
Abdalbasit AM, Mohamed ESM, Ismail H (2017) Tenebrio molitor Mealworm. In Abdalbasit et al. (eds). Unconventional Oilseeds and Oil sources. Academic Press, Elsevier Inc
Aguilar-Miranda ED, Lopez MG, Escamilla-Santana C, de la Barba AP (2002) Characteristics of maize flour tortilla supplemented with ground Tenebrio molitor larvae. J Agric Food Chem 50:192–195. https://doi.org/10.1021/jf010691y
Deen NE, Lamaj S, Verrastro F, Al Bitar V, Baldacchino L F (2021) Effects of two diets on adults’ survival and productivity in mass-rearing of Tenebrio molitor (Coleaoptera: Tenebriodae). J Insects Food Feed 0:1–10. https://doi.org/10.3920/JIFF2020.0129
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 52:285–294. https://doi.org/10.1007/s11745-016-4220-3
Egonyu JP, Kinyuru J, Fombong F, Nganga J, Yusuf AA, Niassy S (2021) Advances in insects for food and feed. Int J Trop Insect Sci 41:1903–1911. https://doi.org/10.1007/s42690-021-00610-8
Farzana T, Mohajan S (2015) Effect of incorporation of soy flour to wheat flour on nutritional and sensory quality of biscuits fortified with mushroom. Food Sci Nutr 3:363–369.https://doi.org/10.1002/fsn3.228
Ghaly AE, Alkoaik FN (2009) The yellow mealworm as a novel source of protein. Am J Agric Biol Sci 4:319–331. https://doi.org/10.3844/ajabssp.2009.319.331
Grau T, Vilcinskas A, Joop G (2017) Sustainable farming of the mealworm Tenebrio molitor for the production of food and feed. Z Naturforsch 72:337–349. https://doi.org/10.1515/znc-2017-0033
Mancini S, Fratini F, Tuccinardi T, Degl’Innocenti C, Paci G (2020) Tenebrio molitor reared on different substrates: is it gluten free? Food Control 110:107014. https://doi.org/10.1016/j.foodcont.2019.107014
Melis R, Braca A, Sanna R, Spada S, Mulas G, Fadda ML, Sassu MM, Serra G, Anedda R (2019) Metabolic response of yellow mealworm larvae to two alternative rearing substrates. Metabolomics 15:1–13. https://doi.org/10.1007/s11306-019-1578-2
Niassy S, Omuse ER, Roos N, Halloran A, Eilenberg J, Egonyu JP, Tanga C, Meutchieye F, Mwangi R, Subramanian S, Musundire R, Nkunika POY, Anankware JP, Kinyuru J, Yusuf A, Ekesi S (2022) Safety, regulatory and environmental issues related to breeding and international trade of edible insects in Africa. Safety. Rev Sci Tech 41(1):117–131. regulatory and environmental issues related to breeding and international trade of edible insects in Africahttps://doi.org/10.20506/rst.41.1.3309
Nowak V, Persijn D, Rittenschober D, Charrondiere UR (2016) Review of food composition data for edible insects. Food chem 193:39–46. https://doi.org/10.1016/j.foodchem.2014.10.114
Payne C, Scarborough P, Rayner MK (2016) Are edible insects more or less ‘healthy’ than commonly consumed meats? A comparison using two nutrient profiling models developed to combat over- and undernutrition. Eur J Clin Nutr 70:285–291. https://doi.org/10.1038/ejcn.2015.149
Poulami A, Malik U, Anandamay B (2016) Oviposition behavior of Callosobruchus maculatus (F.) (Coleoptera: Chrysomelidae: Bruchinae) on four varieties of Lathyrus sativus L. seeds. Entomon 41:1–100377
Quellhorst H, Christos GA, Kun YZ, William RM (2021) The biology, ecology and management of the larger grain borer, Prostephanus truncatus (Horn) (Coleoptera: Bostrichidae). J Stored Prod R 94:101860. https://doi.org/10.1016/j.jspr.2021.101860
RStudio Team, RStudio (2020) RStudio: Integrated Development for R. PBC, Boston, MA URL. http://www.rstudio.com/
Rumbos CI, Karapanagiotidis IT, Mente E, Psofakis P, Athanassiou CG (2020) Evaluation of various commodities for the development of the yellow mealworm, Tenebrio molitor. Sci Rep 10:1–10. https://doi.org/10.1038/s41598-020-67363-1
Rumpold BA, Schlüter OK (2013) Nutritional composition and safety aspects of edible insects. Mol Nutr Food Res 57:802–823. https://doi.org/10.1002/mnfr.201200735
Siemianowska E, Kosewska A, Aljewicz M, Skibniewska KA, Polak-Juszczak L, Jarocki A, Jedras M (2013) Larvae of mealworm (Tenebrio molitor L) as european novel food. Agric Sci 4:287–291. https://doi.org/10.4236/as.2013.46041
Tanga CM, Egonyu JP, Beesigamukama D, Niassy S, Emily K, Magara HJO, Evanson RO, Subramanian S, Ekesi S (2021) Edible insect farming as an emerging and profitable enterprise in East Africa. Cur Opin in Insect Sci 48:64–71. https://doi.org/10.1016/j.cois.2021.09.007
Tucker C (2013) Insects, offal, feet and faces: acquiring new tastes in New Zealand? New Z Sociol 28:101–122
UN (2017) World population projected to reach 9.8 billion in 2050, and 11.2 billion in 2100. United Nations Department of Economic and Social Affairs https://www.un.org/development/desa/en/news/population/world-population-prospects-2017.html. Accessed 15 June 2022
van Huis A, Oonincx DG (2017) The environmental sustainability of insects as food and feed. A review. Agron Sustain Dev 37:1–14. https://doi.org/10.1007/s13593-017-0452-8
van Huis AJ, Van Itterbeeck H, Klunder E, Mertens A, Halloran GM, Vantomme P (2013) Edible insects: future prospects for food and feed security. Food and Agriculture Organization of the United Nations, p 171
van Zyl C, Malan AP (2015) Cost-effective culturing of Galleria mellonella and Tenebrio molitor and entomopathogenic nematode production in various hosts. Afr Entomol 23:361–375. https://doi.org/10.4001/003.023.0232
Acknowledgements
We thank Ms Kitty Stamhuis, Joseph Mabogwane, Estme Msiza and Marna Ferreira for their assistance in maintaining the stock colonies of mealworms. This research was funded in parts through the South African National Research Foundation (NRF) Incentive Funding for Rated Researchers (Grant no. 109380), NRF Research Development Grant for Y- Rated Researchers’ (Grant no. 116347) and the PI grant from the South African Research Chair in Mathematical Models and Methods in Bio-engineering and Biosciences (SARChI M3B2) at the University of Pretoria.
Funding
Open access funding provided by University of Pretoria.
Author information
Authors and Affiliations
Corresponding author
Ethics declarations
Conflict of interest
The authors declare no conflict nor competing interests.
Ethical approval
Not applicable.
Supplementary Information
Table S1 Price per kilogram (kg) of substrates used and their indicative market prices in South Africa Rand (ZAR) and US dollars (US$) *Prices as of July 2021.
Additional information
Publisher’s Note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Electronic supplementary material
Below is the link to the electronic supplementary material.
Rights and permissions
Springer Nature or its licensor (e.g. a society or other partner) holds exclusive rights to this article under a publishing agreement with the author(s) or other rightsholder(s); author self-archiving of the accepted manuscript version of this article is solely governed by the terms of such publishing agreement and applicable law.
Open Access This article is licensed under a Creative Commons Attribution 4.0 International License, which permits use, sharing, adaptation, distribution and reproduction in any medium or format, as long as you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons licence, and indicate if changes were made. The images or other third party material in this article are included in the article’s Creative Commons licence, unless indicated otherwise in a credit line to the material. If material is not included in the article’s Creative Commons licence and your intended use is not permitted by statutory regulation or exceeds the permitted use, you will need to obtain permission directly from the copyright holder. To view a copy of this licence, visit http://creativecommons.org/licenses/by/4.0/.
About this article
Cite this article
Langston, K., Selaledi, L. & Yusuf, A. Evaluation of alternative substrates for rearing the yellow mealworm Tenebrio molitor (L). Int J Trop Insect Sci 43, 1523–1530 (2023). https://doi.org/10.1007/s42690-023-01061-z
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s42690-023-01061-z