State of the Art on Production, Processing and Uses of Meal Worm Tenebrio molitor (Tenebrionidae: Coleoptera)

Author(s)

Prof Dr Sarzamin khan , Dr Amjad Usman , Naseer Ahmad , Parvez Ali , Azaz Ali Shah , Mohammad Israr Abbas ,

Download Full PDF Pages: 184-210 | Views: 309 | Downloads: 90 | DOI: 10.5281/zenodo.5150097

Volume 5 - June 2021 (06)

Abstract

Insects farming is a unique and alternate approach to produce protein rich food and feed. Insects convert organic wastes into biomass, which was successfully used to produce poultry and animal feed.Among the insects,meal worm due to its easy production and high nutritive worth is the best choices to be used as food and feed. This diverse beetle mainlyutilizes different feed products and byproducts, and generally habitatein barns, store, flour mills and grains etc. Its life cycle consists of four developmental stages: the eggs, larva, pupa and at last mature mealworm. The egg to new beetle may take up to 120 days; however, environmental conditions, like temperature, humidity and available diet have been found to reduce its developmental time.Mealworms are omnivorous and can consume all types of animal byproducts such as meat and feathers as well as plant materials. They usually fed on different cereals like wheat, maiz and oats and its bran or flour supplemented with fresh vegetable like potatoes,carrots, lettuce,and other fruits for moisture content with protein supplementation like skimmed milk powder, yeast, or soybean flour.  According to FAO data mealworms have high protein content (13.68 to 22.32 gram per portion of 100 gram) and a significant amount of fatty acids (8.90 to19.94 gram per edible 100-gram portion).  Mealworms are also graded as rich source of zinc and magnesium. Due to its high nutritional worth meal worm has successfully used as animal, poultry and fish feed, immunity enhancer, probiotic and waste degrader. Present review concluded that sustainable meal worm production will be the low cost, easy and environment friendly method to produce cheap but high-quality poultry and fish feed and feed supplements in future. Meal worm farming will be the best choice of rural women livelihood besides its support to poultry and fish feed industry in coming days.  

Keywords

Meal Worm , Tenebrio Molitor 

References

          i            Ada´mkova´, A., L. Kourimska´ , M. Borkovcova´ , M. Kulma and J. Mlˇcek. 2016. Nutritional values of edible Coleoptera (Tenebrio molitor, Zophobasmorio and Alphitobiusdiaperinus) reared in the Czech Republic. Potravinarstvo 10: 663–671.

        ii            Adeniji, A.A., 2007. Effect of replacing groundnut cake with maggot meal in the diet of broilers. International Journal of Poultry Science, 6(11), 822–825.

      iii            Aguilar-Miranda, E.D., López, M.G., Escamilla-Santana, C. and Barba de la Rosa, A.P., 2002. Characteristics of maize flour tortilla supplemented with ground Tenebrio molitor larvae. Journal of Agricultural and Food Chemistry, 50(1), 192–195.

       iv            Alexandratos N, Bruinsma J. World agriculture towards 2030/2050: the 2012 revision. ESA Working paper No. 12-03.

         v            Allen, J.L., Clusella-Trullas, S., Chown, S.L., 2012. The effects of acclimation and rates of temperature change on critical thermal limits in Tenebrio molitor (Tenebrionidae) and Cyrtobagoussalviniae (Curculionidae). J. Insect Physiol. 58, 669–678.

       vi            Alves, A.V., E.J. Sanjinez-Argandona, A.M. Linzmeier, C.A.L. Cardoso and M.L.R. Macedo. 2016. Food value of mealworm grown on Acrocomiaaculeata pulp flour. PLoS One 11: e0151-275. doi: 10.1371/journal.pone.0151-275.

     vii            Anderson S. J. 2000. Increasing calcium levels in cultured insects. Zoo Biol. 19:1–9.

   viii            Baek, S., Perez, A.E., Turcotte, R.M., White, J.B., Adedipe, F., Park, Y.-L., 2015. Response of Tenebrio molitor (Coleoptera: Tenebrionidae) adults to potato: Implications for monitoring and sampling. J. Stored Prod. Res. 60, 5–10.

       ix            Ballitoc, D.A. and Sun, S., 2013. Ground yellow mealworms (Tenebrio molitor L.) feed supplementation improves growth performance and carcass yield characteristics in broilers. Open Science Repository Agriculture, (open-access), p.e23050425.

         x            Barker D, Fitzpatrick MP, Dierenfeld ES. 1998. Nutrient composition of selected whole invertebrates.Zoo Biol 17:123–134.

       xi            Barker D. 1998. Preliminary observations on nutrient composition differences between adult and pinhead crickets, Acheta domestica. BullAssocReptil Amphib Vet 7:10–13.

     xii            Barnes AI, Siva-Jothy MT. 2000. Density-dependent prophylaxis in the mealworm beetle Tenebrio molitorL. (Coleoptera: Tenebrionidae): cuticular melanization is an indicator of investment in immunity. Proc R Soc Lond B Biol Sci :267: 177–82.

   xiii            Barroso, F.G.; de Haro, C.; Sánchez-Muros, M.-J.; Venegas, E.; Martínez-Sánchez, A.; Pérez-Bañón, C. 2014. The potential of various insect species for use as food for fish. Aquaculture, 422–423, 193–201.

   xiv            Belforti, M., Gai, F.,Lussiana, C., Renna, M.,Malfatto, V., Rotolo, L., De Marco, M.,Dabbou, S., Schiavone, A.,Zoccarato, I.,Gasco, L. 2016. Tenebrio molitor meal in rainbow trout (Oncorhynchusmykiss) diets: Effects on animal performance, nutrient digestibility and chemical composition of fillets. Ital. J. Anim. Sci. 14, 4170.

     xv            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 :12:296–313.

   xvi            Benedict P., Brüggen H., ScheibelbergerH. and Jäger H. 2018. Effect of pre‑treatment and drying method on physico‑chemical properties and dry fractionation behaviour of mealworm larvae (Tenebrio molitor L.) Eur Food Res Technol 244:269–280

 xvii            Biasato, I., De Marco, M., Rotolo, L., Renna, M., Lussiana, C., Dabbou, S., Capucchio, M.T., Biasibetti, E., Costa, P., Gai, F. and Pozzo, L., 2016. Effects of dietary Tenebrio molitor meal inclusion in free range chickens. Journal of Animal Physiology and Animal Nutrition, 100(6), 1104–1112.

xviii            Birk, Y., I. Harpaz, I. Ishaaya and A. Bondi. 1962. Studies on the proteolytic activity of the beetles Tenebrio and Tribolium. J. Insect Physiol. 8: 417–429.

   xix            Bovera S, Loponte R, Marono S, Piccolo G, Parisi G, Iaconisi V, et al. 2016. Use of larvae meal as protein source in broiler diet: effect on growth performance, nutrient digestibility, and carcass and meat traits. J Anim Sci. 94:639–47.

     xx            Brewer, M.S. 2012. Reducing the fat content in ground beef without sacrificing quality: A review. Meat. Sci. : 91, 385–395.

   xxi            Calislar, S. 2017. Nutrient content of mealworms Tenebrio molitor L. and the utilization possibilities in poultry nutrition. In Proceedings of the International Conference on Agriculture, Forest, Food Sciences and Technologies (ICAFOF), Cappadocia, Turkey, 15–17.

 xxii            Chae J-H, Kurokawa K, So Y-I, Hwang HO, Kim M-S, Park J-W, et al. 2012. Purification and characterization of tenecin 4, a new anti-Gram-negative bacterial peptide, from the beetle Tenebrio molitor Dev Comp Immunol :36:540–6.

xxiii            Connat, J.L., Delbecque, J.P., Glitho, I., Delachambre, J., 1991. The onset of metamorphosis in Tenebrio molitor larvae (Insecta, Coleoptera) under grouped, isolated and starved conditions. J. Insect Physiol. 37. doi:10.1016/0022-1910(91)90042-X

xxiv            Cossins, A.R., Bowler, K., 1987. Temperature Biology of Animals. Springer, NL.Davenport, J., 1992. Animal Life at Low Temperatures. Springer, UK. DeFoliart, G.R., 1989. The human use of insects as food and as animal feed. Bull. Entomol.Soc. Am. 35, 22–35

  xxv            Cotton, R.T. 1927. Notes on the biology of the mealworms Tenebrio molitor L. and T. obscurus Fab. Ann. Entomol. Soc. Am. 20: 81–86. doi: 10.1093/aesa/20.1.81.

xxvi            Davis, G. 1970a. Protein nutrition of “Tenebrio molitor” L. XII. Effects of dietary casein concentration and of dietary cellulose on larvae of race F. Arch. Int. Physiol. Biochim. 78: 37–41. doi: http://dx.doi.org/10.3109/13813457009075180.

xxvii            Davis, G. 1970b. Protein nutrition of “Tenebrio molitor” L. XIII. Consideration of some dietary factors of casein, lactalbumin, and lactalbumin hydrolysate. Arch. Int. Physiol. Biochim. 78: 467–473. doi: 10.3109/13813457009075197.

xxviii            Davis, G. 1974. Protein nutrition of Tenebrio molitor L: XVII. Improved amino acid mixture and interaction with dietary carbohydrate. Arch. Int. Physiol. Biochem. 82: 631–637. doi: 10. 3109/13813457409072315.

xxix            Davis, G. and J. Leclercq. 1969. Protein nutrition of “Tenebrio molitor” L. IX. Replacement caseins for the reference diet and a comparison of the nutritional values of various lactalbumins and lactalbumin hydrolysates. Arch. Int. Physiol. Biochim. 77: 687–693.

  xxx            Davis, G.R., 1978. Growth response of larvae of Tenebrio molitor L. to concentrations of dietary amino acids. J. Stored Prod. Res. 14, 69–71.

xxxi            Dick, J., 2008. Oviposition in Certain Coleoptera. Ann. Appl. Biol. 24, 762–796.

xxxii            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.

xxxiii            FAO. The State of World Fisheries and Aquaculture 2018—Meeting the Sustainable Development Goals; The Food and Agricultural Organization of the United Nations: Rome, Italy, 2018; p. 227.

xxxiv            Finke MD. 2002.  Complete nutrient composition of commercially raised invertebrates used as food for insectivores. Zoo Biol, 21:269–85.

xxxv            Finke, M.; D. Winn (2004). "Insects and related arthropods: A nutritional primer for rehabilitators". Journal of Wildlife Rehabilitation. 27: 14–17.

xxxvi            Fiore, C., 1960. Effects of temperature and parental age on the life cycle of the dark mealworm, Tenebrio obscurus Fabricius. Journal of the New York Entomological Society, 68(1), 27–35.

xxxvii            Fraenkel, G. 1950. The nutrition of the mealworm, Tenebrio molitor L. (Tenebrionidae, Coleoptera). Physiol. Zool. 23: 92–108.

xxxviii            Franco, D.; González, L.; Bispo, E.; Rodríguez, P.; Garabal, J.I.; Moreno, T. 2010. Study of hydrolyzed protein composition, free amino acid, and taurine content in di_erent muscles of galician blonde beef. J. Muscle Foods :21, 769–784.

xxxix            Friedrich, J.P.; List, G.R. 1982. Characterization of soybean oil extracted by supercritical carbon dioxide and hexane. J. Agric. Food Chem. 30, 192–193.

       xl            Gatlin, D., Barrows, F., Brown, P.,Dabrowski, K., Gaylord, T., Hardy, R., Herman, E., Hu, G.,Krogdahl, A.,Nelson, R. 2007. Expanding the utilization of sustainable plant products in aquafeeds: A review. Aquac. Res., 38, 551–579.

     xli            Gerber, G.H. and D.U. Sabourin. 1984. Oviposition site selection in Tenebrio molitor (Coleoptera: Tenebrionidae). Can. Entomol. 116: 27–39.

   xlii            Ghaly, a. E., Alkoaik, F.N., American Journal of Agricultural and Biological Sciences, 2009. The Yellow Mealworm as a Novel Source of Protein. Am. J. Agric. Biol. Sci. 4, 319–331. doi:10.3844/ajabssp.2009.319.331

 xliii            Ghosh, K.; Ray, A.K.; Ringø, E. 2018. Applications of plant ingredients for tropical and subtropical freshwater finfish: Possibilities and challenges. Rev. Aquacult., in press. [CrossRef]

 xliv            Giri SS, Sen SS, Sukumaran V. 2012. Effects of dietarysupplementationof potential probiotic PseudomonasaeruginosaVSG-2 on the innate immunity and disease resistanceof tropical freshwater fish, Labeorohita. Fish Shellfishimmunol; 32:1135–40.

   xlv            Gustavsson J, Cederberg C, Sonesson U. 2011. Global food losses and food waste: extent, causes and prevention; study conducted for the International Congress Save Food! at Interpack. Düsseldorf, Germany, Food and Agricul Orgof the United Nations, Rome, 16–17  ,

 xlvi            Hai NV, Buller N, Fotedar R. 2009. Effects of probiotics (Pseudomonassynxanthaand Pseudomonas aeruginosa) on the growth, survival, and immune parameters of juvenile western kingprawns (PenaeuslatisulcatusKishinouye, 1896). Aquac Res. 40:590–602.

xlvii            Hardouin, J.; Mahoux, G., 2003. Zootechnied’insectes – Elevage et utilisation au bénéfice de l'homme et de certainsanimaux. Bureau pour l’Echange et la Distribution de l’Information sur le Mini-élevage (BEDIM), 164 p.

xlviii            Harrell, P.E. and Bailer, J., 2004. Pass the mealworms, please: Using mealworms to develop science process skills. Science Activities: Classroom Projects and Curriculum Ideas, 41(2), 31–36.

 xlix            Hasan MR. Rana KJ, Siriwardena S. 2009. Impact of rising feed ingredient prices on aquafeeds and aquaculture production, Food and AgriculOrgof the United Nations, Rome. 11-15 p

          l            Havenaar R, Veld JH. 1992. Probiotics: a general view. In: WoodBJ, editor. The lactic acid bacteria, volume 1. US: Springer,;151–70.

        li            Henry, M.; Gasco, L.; Piccolo, G.; Fountoulaki, E. 2015. Review on the use of insects in the diet of farmed fish: Past and future. Anim. Feed Sci. Technol., 203, 1–22. 2014

      lii            Hill, D.S. 2002. Pests: Class Insecta. Pp. 135–315. In Pests of Stored Foodstuffs and Their Control. Springer, Dordrecht, the Netherlands. doi: https://doi.org/10.1007/0-306-48131-6_14.

    liii            Houbraken, M., Spranghers, T., De Clercq, P., Cooreman-Algoed, M., Couchement, T., De Clercq, G., Verbeke, S., Spanoghe, P., 2016. Pesticide contamination of Tenebrio molitor (Coleoptera: Tenebrionidae) for human consumption. Food Chem. 201, 264–269. doi:10. 1016/j.foodchem.2016.01.097

     liv            House J. 2016. Consumer acceptance of insect-based foods in the Netherlands: academic and commercial implications. Appetite; 107:47–58.

       lv            Hussain, I., Khan, S., Sultan, A., Chand, N., Khan, R., Alam, W., & Ahmad, N. 2017. Meal worm (Tenebrio molitor) as potential alternative source of protein supplementation in broiler. Int. J. Biosci, 10, 255-262.

     lvi            Hwangbo, J.; Hong, E. C.; Jang, A.; Kang, H. K.; Oh, J. S.; Kim,B. W. and Park, B. S. 2009. Utilization of house fly-maggots, a feed supplement in the production of broiler chickens. Journal of Environmental Biology 30:609-614

   lvii            Iaconisi, V.,Marono, S., Parisi, G., Gasco, L., Genovese, L.,Maricchiolo, G., Bovera, F. and Piccolo, G., 2017. Dietary inclusion of Tenebrio molitor larvae meal: Effects on growth performance and final quality treats of blackspot sea bream (Pagellusbogaraveo). Aquaculture, 476, 49–58.

 lviii            Islam MM, Yang C-J. 2017. Efficacy of mealworm and super mealworm larvae probiotics as an alternative to antibiotics challenged orally with Salmonella and E. coli infection in broiler chicks. PoultSci;96:27–34.

     lix            Jin XH, Heo PS, Hong JS, Kim NJ, Kim YY. 2016. Supplementation of dried mealworm (Tenebrio molitor larva) on growth performance, nutrient digestibility and blood profiles in weaning pigs. Asian-Australas J AnimSci;29:979–86.

       lx            John, A.M., Davis, G.R., Sosulski, F.W., 1978. Protein nutrition of Tenebrio molitor L. XIX. Growth response to levels of dietary protein and of an amino acid mixture. Arch.Int.PhysiolBiochim. 86, 761–770.

     lxi            John, A.M., G.R. Davis and F.W. Sosulski. 1979. Protein nutrition of Tenebrio molitor L. XX. Growth response of larvae to graded levels of amino acids. Arch. Int. Physiol. Biochim. 87:997–1004. doi: 10.3109/13813457909070548.

   lxii            Jones LD, Cooper RW, Harding RS. 1972. Compositionof mealworm Tenebrio molitor larva. J. Zoo Anim Med 3:34–41.

 lxiii            Jongema Y. 2015. List of edible insect species of the world. The Netherlands: Laboratory of Entomology, Wageningen University; available at http://wwwentwurnl/UK/Edible+insects/Worldwide+species+list/2015.

 lxiv            Jordan, Rob. 2015. Plastic-eating worms may offer solution to mounting waste, Stanford researchers discover". Stanford News Service. Stanford News Service.

   lxv            Jun. K. Jun, H. Kim, K. Lee, H. Paik, J. Kang. 2002. Characterization of Bacillus polyfermenticus SCD as a probiotic Korean J. Microbiol. Biotechnol., 30, p. 359 366

 lxvi            Khan, S., Naz, S., Sultan, A., Alhidary, I.A.,Abdelrahman, M.M., Khan, R.U., Khan, N.A., Khan, M.A. and Ahmad, S., 2016.Worm meal: a potential source of alternative protein in poultry feed. World'sPoultry Science Journal, 72(1), 93–102.

lxvii            Khempaka, S., Chitsatchapong, C. and Molee, W., 2011. Effect of chitin and protein constituents in shrimp head meal on growth performance, nutrient digestibility, intestinal microbial populations, volatile fatty acids, and ammonia production in broilers. Journal of Applied Poultry Research, 20(1), 1–11

lxviii            Khosrava, S.; Kim, E.; Lee, Y.-S.; Lee, S.M. 2018 Dietary inclusion of mealworm (Tenebrio molitor) meal as an alternative protein source in practical diets for juvenile rockfish (Sebastes schlegeli). Entomol. research 48, 214–221.

 lxix            Kim, S.Y., Park, J.B., Lee, Y.B., Yoon, H.J., Lee, K.Y. and Kim, N.J., 2015. Growth characteristics of mealworm Tenebrio molitor. Journal of Sericultural and Entomological Science, 53(1), 1–5

   lxx            Kingsolver, J.G., Higgins, J.K., Augustine, K.E., 2015. Fluctuating temperatures and ectothermgrowth: distinguishing non-linear and time-dependent effects. J. Exp. Biol.218, 2218–2225.

 lxxi            Klasing, K. C. ; Thacker, P. ; Lopez, M. A. ; Calvert, C. C., 2000. Increasing the calcium content of mealworms (Tenebrio molitor) to improve their nutritional value for bone mineralization of growing chicks. J. Zoo Wildlife Med., 31 (4): 512-517

lxxii            Koo, H., S. Kim, H. Oh, J. Kim, D. Choi, D. Kim and I. Kim. 2013. Temperature-dependent development model of larvae of mealworm beetle, Tenebrio molitor L. (Coleoptera: Tenebrionidae). Korean J. Appl. Entomol. 52: 387–394. doi: 10.5656/KSAE.2013.11.0.066.

lxxiii            Kröncke, N.; Grebenteuch, S.; Keil, C.; Demtröder, S.; Kroh, L.; Thünemann, A.F.; Benning, R.; Haase, H. 2018. Effect of different drying methods on nutrient quality of the yellow mealworm (Tenebriomolitor L.). Insects, 10, 84.

lxxiv            Lardies, M. a, Arias, M.B., Poupin, M.J., Bacigalupe, L.D., 2014. Heritability of hsp70 expression in the beetle Tenebrio molitor: Ontogenetic and environmental effects. J. InsectPhysiol. 67, 70–5. doi:10.1016/j.jinsphys.2014.06.005

lxxv            LeBlanc JG, Milani C, deGiori GS, Sesma F, van Sinderen D, Ventura M. 2013. Bacteria as vitamin suppliers to their host: a gutmicrobiota perspective. CurrOpinBiotechnol; 24: 160–8.

lxxvi            Leclercq, J. 1948. Sur les besoinsnutritifs de la larve de Tenebrio molitor L. Biochim. Biophys. Acta 2: 2–5. doi: 10.1016/0006-3002(48)90046-8.

lxxvii            Lee, K.C.; Lee, S.K.; Kim, H.K. 2016. Chemical compositions of the four lines of Korean native chickens. Korean J. Poult. Sci., 43, 119–128.

lxxviii            Lensvelt EJ, Steenbekkers LP. 2014. Exploring consumer acceptance of entomophagy: a survey and experiment in Australia and the Netherlands. Ecol Food Nutr. 53:543–61.

lxxix            Li L, Xie B, Dong C, Hu D, Wang M, Liu G., 2015. Rearing Tenebrio molitor L. (Coleptera: Tenebrionidae) in the “Lunar Palace 1” during a 105-day multi-crew closed integrative BLSS experiment. Life Sci Space Res 2015;7: 9–14.

lxxx            Li, L., Zhao, Z. and Liu, H., 2013. Feasibility of feeding yellow mealworm (Tenebrio molitor L.) in bioregenerative life support systems as a source of animal protein for humans. Acta Astronautica, 92(1), 103–109.

lxxxi            Lockwood and Deirdre. 2019. "Mealworms Munch Polystyrene Foam"Chemical and Engineering News.

lxxxii            Ludwig, D. 1956. Effects of temperature and parental age on the life cycle of the mealworm, Tenebrio molitor Linnaeus (Coleoptera, Tenebrionidae). Ann. Entomol. Soc. Am. 49: 12– 15.

lxxxiii            Lv, X., Liu, C., Li, Y., Gao, Y., Wang, H., Li, J., Guo, B., 2014. Stereoselectivity in bioaccumulation and excretion of epoxiconazole by mealworm beetle (Tenebrio molitor) larvae. Ecotoxicol. Environ. Saf. 107C, 71–76.

lxxxiv            Lwalaba, D.; Ho_mann, K.H.;Woodring, J. 2010. Control of the release of digestive enzymes in the larvae of thefall armyworm, Spodopterafrugiperda. Arch. Insect Biochem. Physiol. 73, 14–29.

lxxxv            Lyon, W. F. Yellow and dark mealworms; Entomology, OhioState University Extension, 1991; http://www.ag.ohio-state.edu/_ohioline/hyg-faxt/2000/29093.html.

lxxxvi            Manojlovic, B. 1987. A contribution of the study of the influence of the feeding of imagos and of climatic factors on the dynamics of oviposition and on the embryonal development of yellow mealworm Tenebrio molitor L. (Coleoptera: Tenebrionidae). Zasˇtitabilja 38: 337–348. doi: 10.7852/jses.2012.50.2.126

lxxxvii            Martin RD, Rivers JPW, Cowgill UM. 1976. Culturingmealworms as food for animals in captivity.Int Zoo Yearb 16:63–70.

lxxxviii            Martin, H.E. and L. Hare. 1942. The nutritive requirements of Tenebrio molitor larvae. Biol. Bull. 83: 428–437. doi: 10.2307/1538240.

lxxxix            Martin, H.E., Hare, L., 1941. The Nutritive Requirements of Tenebrio Molitor 428–437.

     xc            Mellandby, K. and R.A. French. 1958. The importance of drinking water to larval insects. Entomol. Exp. Appl. 1: 116–124. doi: 10.1111/j.1570-7458.1958.tb00014.x.

   xci            Menezes, C.W.G. de, Camilo, S. da S., Fonseca, A.J., Assis Júnior, S.L. de, Bispo, D.F., Soares, M.A., 2014. A dietaalimentar da presa Tenebrio molitor (Coleoptera: Tenebrionidae) podeafetar o desenvolvimento do predadorPodisusnigrispinus (Heteroptera: Pentatomidae)? Arq. Inst. Biol. (Sao. Paulo). 81, 250–256. doi:10.1590/1808-1657001212012

 xcii            Miglietta, P.; De Leo, F.; Ruberti, M.; Massari, S. 2015. Mealworms for food: A water footprint perspective. Water, 7, 6190–6203. [CrossRef]

xciii            Miryam,D., Bar, P.S.T.,Oscherov,M.E., 2000. CiclodeVida de Tenebrio molitor (Coleoptera, Tenebrionidae) enCondicionesExperimentales. Methods.

xciv            Morales-Ramos, J.A., M.G. Rojas, D.I. Shapiro-Ilan and W.L. Tedders. 2011. Self selection of two diet components by Tenebrio molitor (Coleoptera: Tenebrionidae) larvae and its impact on fitness. Environ. Entomol. 40: 1285–94. doi: 10.1603/EN10239.

  xcv            Morales-Ramos, J.A., M.G. Rojas, D.I. Shapiro-Ilan and W.L. Tedders. 2010. Developmental plasticity in Tenebrio molitor (Coleoptera: Tenebrionidae): Analysis of instar variation in number and development time under different diets. J. Entomol. Sci. 45: 75–90. doi: 10.18474/0749-8004-45.2.75.

xcvi            Morales-Ramos, J.A., M.G. Rojas, D.I. Shapiro-llan and W.L. Tedders. 2013. Use of nutrient self-selection as a diet refining tool in Tenebrio molitor (Coleoptera: Tenebrionidae). J. Entomol. Sci. 48: 206–221. doi: 10.18474/0749-8004-48.3.206.

xcvii            Morales-Ramos, J.A., Rojas, M.G., Kay, S., Shapiro-Ilan, D.I., Tedders, W.L., 2012. Impact of Adult Weight, Density, and Age on Reproduction of Tenebrio molitor (Coleoptera: Tenebrionidae). J. Entomol. Sci. 47, 208–220. doi:10.18474/0749-8004-47.3.208

xcviii            Morales-Ramos, J.A., Rojas, M.G., Shapiro-Ilan, D.I., 2013a. Introduction, in: Mass Production of Beneficial Organisms: Invertebrates and Entomopathogens. pp. 1–15. doi:10.1007/s13398-014-0173-7.2

xcix            Morales-Ramos, J.A., Rojas, M.G., Shelby, K.S., Coudron, T.A., 2015b. Nutritional Value of Pupae Versus Larvae of Tenebrio molitor (Coleoptera: Tenebrionidae) as Food for Rearing Podisusmaculiventris (Heteroptera: Pentatomidae). J. Econ. Entomol. tov338. doi:10.1093/jee/tov338

         c            Murray, D.R.P., 1960. The stimulus to feeding in larvae of Tenebrio molitor L. J. Insect Physiol. 4, 80–91. doi:10.1016/0022-1910(60)90069-X

       ci            Murray, D.R.P., 1968. The Importance of water in the normal growth of larvae of Tenebrio molitor. Entomol. Exp. Appl. 11, 149–168. doi:10.1017/CBO9781107415324.004

     cii            Mutchmor, J.A. and A.G. Richards. 1961. Low temperature tolerance of insects in relation to the influence of temperature on muscle apyrase activity. J. Insect Physiol. 7: 141–158. doi:10.1016/0022-1910(61)90051-8.

   ciii            Ng, W. K. ; Liew, F. L. ; Ang, L. P. ; Wong, K. W., 2001. Potential of mealworm (Tenebrio molitor) as an alternative protein source in practical diets for African catfish, Clariasgariepinus. Aquacult. Res., 32 (Supplement 1): 273-280

   civ            Nowak V, Persijn D, Rittenschober D, Charrondiere UR. Review of food composition data for edible insects. Food Chem 2016;193:39–46.

     cv            Nuno R., Abelho M., and Costa R. 2017. A Review of the Scientific Literature for Optimal Conditions for Mass Rearing Tenebrio molitor (Coleoptera: Tenebrionidae). Journal of Entomological Science, 53(4):434-454. https://doi.org/10.18474/JES17-67.1 URL: http://www.bioone.org/doi/full/10.18474/JES17-67.1

   cvi            Oelschlaeger TA. 2010. Mechanisms of probiotic actions—a review.Int J Med Microbiol;300:57–62.

 cvii            Olsen, R.L.; Hasan, M.R. 2012. A limited supply of fishmeal: Impact on future increases in global aquaculture production. Trends Food Sci. Technol. 27, 120–128. [CrossRef]

cviii            Oonincx DG, de Boer IJ. 2012. Environmental impact of the production of mealworms as a protein source for humans—a life cycle assessment. PLoS One;7:e51145.

   cix            Oonincx DG, van Itterbeeck J, Heetkamp MJ, van den Brand H, van Loon JJ, van Huis A. 2010. An exploration on greenhouse gas and ammonia production by insect species suitable for animal or human consumption. PLoS One;5:e14445.

     cx            Oonincx, D.G., Van Broekhoven, S., Van Huis, A. and van Loon, J.J.,2015. Feed conversion, survival and development, and compositionof four insect species on diets composed of food by-products. PLoSOne, 10(12), p.e0144601. doi: 10.1371/journal.pone.0144601.

   cxi            Park, J.B., W.H. Choi, S.H. Kim, H.J. Jin, Y.S. Han and N.J. Kim. 2014. Developmental characteristics of Tenebrio molitor larvae (Coleoptera: Tenebrionidae) in different instars. Int. J. Ind. Entomol. 28: 5–9. doi: http://dx.doi.org/10.7852/ijie.2014.28.1.5.

 cxii            Payne CL, Scarborough P, Rayner M, Nonaka K. 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;70:285–91.

cxiii            Piccolo, G.; Iaconisi, V.; Marono, S.; Gasco, L.; Loponte, R.; Nizza, S.; Bovera, F.; Parisi, G. 2017. Effect of Tenebriomolitor larvae meal on growth performance, in vivo nutrients digestibility, somatic and marketable indexes of gilthead sea bream (Sparusaurata). Anim. Feed Sci. Technol., 226, 12–20. [CrossRef]

cxiv            Pölkki, M., Krams, I., Kangassalo, K. and Rantala, M.J., 2012. Inbreeding affects sexual signalling in males but not females of Tenebrio molitor. Biology Letters, p.rsbl20111135. 247-276.

  cxv            Punzo, F. and J.A. Mutchmor. 1980. Effects of temperature, relative humidity and period of exposure on the survival capacity of Tenebrio molitor (Coleoptera: Tenebrionidae). J. Kansas Entomol. Soc. 53: 260–270. doi: 10.2307/25084029.

cxvi            Ramos-Elorduy, J. ; Avila Gonzalez, E. ; Rocha Hernandez, A. ; Pino, J. M., 2002. Use of Tenebrio molitor (Coleoptera: Tenebrionidae) to recycle organic wastes and as feed for broiler chickens. J. Econ. Entomol., 95 (1): 214-220

cxvii            Ramos-Elorduy, J. 1997. Insects: A sustainable source of food? J. Ecol. Food Nut. 36: 247-276.

cxviii            Ramos-Elorduy, J., and J. M. Pino. 1990. Variation de lavaleur nutritive de Tenebrio molitor L.E ´ le´ve´ sur different substrats. Proc. Int. Working Conf. Stored Prod. Protect. 1: 210 - 210.

cxix            Ravzanaadii, N., Kim, S.H., Choi,W.H., Hong, S.J. and Kim, N.J., 2012. Nutritional value of mealworm, Tenebriomolitoras food source. International Journal of Industrial Entomology, 25(1), 93–98.

  cxx            Rho, M.S. and K.P. Lee. 2014. Geometric analysis of nutrient balancing in the mealworm beetle, Tenebrio molitor L. (Coleoptera: Tenebrionidae). J. Insect Physiol. 71: 37–45. doi:10.1016/j.jinsphys.2014.10.001.

cxxi            Ringo E, Zhou Z, Olsen RE, Song SK. 2012. Use of chitin and krill inaquaculture – the effect on gut microbiota and the immunesystem: a review. AquacNutr;18:117–31.

cxxii            Rossi M, Amaretti A, Raimondi S. 2011. Folate production by probiotic bacteria. Nutrients;3:118–34.

cxxiii            Rueda, L.M., Axtell, R.C., 1996. Temperature-dependent development and survival of theLesser Mealworm, Alphitobiusdiaperinus. Med. Veter. Entomol. 10, 80–86.

cxxiv            Rumpold BA, Schlüter . 2013. Nutritional composition and safety aspects of edible insects. Mol Nutr Food Res;57:802–23.

cxxv            Schiavone, G., Raskovic, D., Greco, J., &Abeni, D. 2014. Platelet-rich plasma for androgenetic alopecia: a pilot study. Dermatologic Surgery, 40(9), 1010-1019.

cxxvi            Schlüter O, Rumpold B, Holzhauser T, Roth A, Vogel RF, Quasigroch W, et al. Safety aspects of the production of foods and food ingredients from insects. Mol Nutr Food Res 2016:1–14.

cxxvii            Schmidt, Anatol; Call, Lisa; Macheiner, Lukas; Mayer, Helmut K. 2018. "Determination of vitamin B12 in four edible insect species by immunoaffinity and ultra-highperformance liquid chromatography". Food Chemistry. 281: 124–129. doi:10.1016/j.foodchem.2018.12.039PMID 30658738

cxxviii            Shapiro-Ilan, D., M.G. Rojas, J.A. Morales-Ramos, E.E. Lewis and W.L. Tedders. 2008. Effects of host nutrition on virulence and fitness of entomopathogenic nematodes: Lipidand protein-based supplements in Tenebrio molitor diets. J. Nematol. 40: 13–9.

cxxix            Simon, E., Baranyai, E., Braun, M., Fábián, I. and Tóthmérész, B., 2013. Elemental concentration in mealworm beetle (Tenebriomolitor L.) during metamorphosis. Biological Trace Element Research, 154(1),81–87

cxxx            Slater, M.; D‘Abramo, L.; Engle, C.R. 2018. Aquaculture Research Priorities for the Next Decade: A Global Perspective. J. World Aqua. cult. Soc., 49, 3–6. [CrossRef]

cxxxi            Smetana, S.; Schmitt, E.; Mathys, A. 2019. Sustainable use of Hermetiaillucens insect biomass for feed and food: Attributional and consequential life cycle assessment. Resour. Conserv. Recycl., 144, 285–296. [CrossRef]

cxxxii            Song SK, Beck BR, Kim D, Park J, Kim J, Kim HD, 2014.Pre biotics as immune stimulants in aquaculture: a review. Fish Shell fish Immunol;40:40–8.

cxxxiii            Spencer, W. and J. Spencer. 2006. Management guideline manual for invertebrate live food species. EAZA Terr. Invertebr. TAG. 1–54.

cxxxiv            Springmann M, Godfray HC, Rayner M, Scarborough P. 2016. Analysis and valuation of the health and climate change cobenefits of dietary change. Proc Natl AcadSci;113:4146–51.

cxxxv            Tang, Q., Dai, Y., Zhou, B., 2012. Regulatory effects of Tenebrio molitor Linnaeus on immunological function in mice. African J. Biotechnol. 11, 8348–8352. doi:10.5897/AJB12.340

cxxxvi            Thévenot, A.; Rivera, J . L.; Wilfart, A.; Maillard, F.; Hassouna, M.; Senga-Kiesse, T.; Le Féon, S.; Aubin, J., 2018. Mealworm meal for animal feed: Environmental assessment and sensitivity analysis to guide future prospects. J. Cleaner Prod., 170 (1): 1260-1267

cxxxvii            Tilman D, Clark M. Global diets link environmental sustainability and human health. Nature 2014;515:518–22.

cxxxviii            Tracey, K.M., 1958. Effects of parental age on the life cycle of the mealworm, Tenebrio molitor Linnaeus. Annals of the Entomological Society of America, 51(5), 429–432.

cxxxix            Tran G., Gnaedinger C., Mélin C., 2019. Mealworm (Tenebrio molitor). Feedipedia, a programme by INRA, CIRAD, AFZ and FAO. https://www.feedipedia.org/node/16401

   cxl            Urrejola, S., Nespolo, R., Lardies, M.A., 2011. Diet-induced developmental plasticity in life histories and energy metabolism in a beetle. Rev. Chil. Hist. Nat. 84, 523–533. doi:10.4067/S0716-078X2011000400005

 cxli            Urs, K.C.D. and T.L. Hopkins. 1973b. Effect of moisture on growth rate and development of two strains of Tenebrio molitor L. (Coleoptera, Tenebrionidae). J. Stored Prod. Res. 8: 291–297. doi: 10.1016/0022-474X(73)90045-3.

cxlii            Van Broekhoven, S., D.G.A.B. Oonincx, A. van Huis and J.J.A. van Loon. 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. doi: 10.1016/j.jinsphys.2014.12.005

cxliii            Vvan Broekhoven, S., Oonincx, D.G.A.B., van Huis, A., van Loon, J.J.A., 2014. Growthperformance and feed conversion efficiency of three edible mealworm species(Coleoptera: Tenebrionidae) on diets composed of organic by-products. J. Insect Physiol. 73, 1–10.

cxliv            Van der Klis, J. D., and A. J. M. Jansman. 2002. Optimisingnutrient digestion, absorption and gut barrier function inmonogastrics: Reality or illusion? Nutritionand Health of the Gastrointestinal Tract. Wageningen Academic Publishers, Wagen-ingen, The Netherlands. Pages 15–36

cxlv            Van Huis A. 2016. Edible insects are the future? Proc NutrSoc;75:294–305.

cxlvi            Van Huis, A.; Oonincx, D.G.A.B. 2017. The environmental sustainability of insects as food and feed. A review. Agron. Sustain. Dev., 37, 43. [CrossRef]

cxlvii            Van Zyl, C. and Malan, A.P., 2015. Cost-effective culturing of Galleria mellonella and Tenebrio molitor and entomopathogenic nematode production in various hosts. African Entomology, 23(2), 361–375.

cxlviii            Veldkamp, T. ; van Duinkerken, G. ; van Huis, A. ; Lakemond, C. M. M. ; Ottevanger, E. ; Bosch, G. ; van Boekel, M. A. J. S., 2012. Insects as a sustainable feed ingredient in pig and poultry diets - a feasibility study. Wageningen Livestock Research. Rapport 638

cxlix            Verbeke W, Spranghers T, De Clercq P, De Smet S, Sas B, Eeckhout M. 2015. Insects in animal feed: acceptance and its determinants among farmers, agriculture sector stakeholders and citizens. Anim Feed Sci Technol. 204:72–87.

       cl            Wan LY, Chen ZJ, Shah NP, El-Nezami H. 2016. Modulation of intestinalepithelial defense responses by probiotic bacteria. CritRevFoodSciNutr;56:2628–41.

     cli            Wang Xuegui, Zheng Xiaowei, Li Xiaoyu, Yao Jianming, Jiang Surong, Z.M., 2010. Study on the Biological Characters of Tenebrio molitor L. Chin. Agr. Sci. Bull. 230–233.

   clii            Wang YingChang ; Chen YunTang ; Li XingRui ; Xia JunMing ; Du QinSheng ; ZhiChang'an, 1996. Study on rearing the larvae of Tenebrio molitor Linne and the effects of its processing and utilization. Acta Agriculturae Universitatis Henanensis, 30 (3): 288-292

 cliii            Wang, J., Yun, B., Xue, M.,Wu, X., Zheng, Y. and Li, P., 2012. Apparent digestibility coefficients of several protein sources, and replacement of fishmeal by porcine meal in diets of Japanese seabass, Lateolabrax japonicus, are affected by dietary protein levels. Aquaculture Research, 43(1), 117–127.

 cliv            Weaver, D.K. and J.E. McFarlane. 1990. The effect of larval density on growth and development of Tenebrio molitor. J. Insect Physiol. 36: 531–536.

   clv            Yang-Ju Son, Soo Young Choi, In-Kyeong Hwang, Chu Won Nho and Soo Hee Kim. 2020. Could Defatted Mealworm (Tenebrio molitor) and Mealworm Oil Be Used as Food Ingredients?. Foods. 1-13;

 clvi            Zhao, X.; Vázquez-Gutiérrez, J.L.; Johansson, D.P.; Landberg, R.; Langton, M.2016.  Yellow mealworm protein for food purposes-Extraction and functional properties. PLoS ONE, 11, e0147791. [CrossRef] [PubMed]

clvii            Zielin´ska, E., B. Baraniak, M. Karas, K. Rybczyn´ ska and A. Jakubczyk. 2015. Selected species of edible insects as a source of nutrient composition. Food Res Int. 77(3): 460– 466.

Cite this Article: