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http://dx.doi.org/10.1186/s41610-021-00212-y

Honey bees and their brood: a potentially valuable resource of food, worthy of greater appreciation and scientific attention  

Ghosh, Sampat (Agriculture Science and Technology Research Institute, Andong National University)
Meyer-Rochow, Victor Benno (Agriculture Science and Technology Research Institute, Andong National University)
Jung, Chuleui (Agriculture Science and Technology Research Institute, Andong National University)
Publication Information
Journal of Ecology and Environment / v.45, no.4, 2021 , pp. 293-304 More about this Journal
Abstract
Despite the consumption of bee brood in several parts of the world, particularly in the tropical areas, the practice has received comparatively little attention. We have reviewed all the available information on the nutrient composition and functional properties of different developmental stages of honey bee workers belonging to different species and subspecies. Noticing the competent nutrient composition of, in particular, honey bee brood, pupae, and prepupae, we suggest that they could be a potential source of human nutrition as well as animal feed. Moreover, drone brood is an ideal candidate for use as a food or as food ingredient. However, to analyze the functional properties of different honey bee species remains a task for further analysis.
Keywords
Entomophagy; Protein; Amino acid; Minerals; Functional properties; Apiary; Bee products;
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1 Ramos-Elorduy J, Moreno JMP, Prado EE, Perez MA, Otero JL, de Guavara OL. Nutritional value of edible insects from the state of Oaxaca, Mexico. J Food Compos Anal. 1997;10(2):142-57. https://doi.org/10.1006/jfca.1997.0530.   DOI
2 Chang NC, Hung SI, Hwa KY, Kato I, Chen JE, Liu CH, et al. A macrophage protein, Ym1, transiently expressed during inflammation is a novel mammalian lectin. J Biol Chem. 2001;276(20):17497-506. https://doi.org/10.1074/jbc.M010417200.   DOI
3 DeFoliart G. Insects as human food. Crop Prot. 1992;11(5):395-9. https://doi.org/10.1016/0261-2194(92)90020-6.   DOI
4 DeFoliart G. Edible insects as minilivestock. Biodivers Conserv. 1995;4(3):306-21. https://doi.org/10.1007/BF00055976.   DOI
5 Finke MD. Nutrient composition of bee brood and its potential as human food. Ecol Food Nutr. 2005;44(4):257-70. https://doi.org/10.1080/03670240500187278.   DOI
6 Gessain M, Kinzler T. MieletInsectes a miel chez les Bassari et D'autres Populations du Senegal Oriental [Honey and Honey Making Insects in the Bassari and Other Populations of Eastern Senegal]. In L'hommeetL'annimal; PujolR, Ed.; Premier Colloqued'Ethnozoologie: Paris, France, 1975; pp. 247-254.
7 Onore G. A brief note on edible insects in Ecuador. Ecol Food Nutr. 1997;36(2-4):277-85. https://doi.org/10.1080/03670244.1997.9991520.   DOI
8 Vasilenko YK, Klishina II, Lazaryan DS. A comparative study of the immunotropic and hepatotropic action of beekeeping products in rats with drug-induced hepatitis. Pharm Chem J. 2005;39:319-22. https://doi.org/10.1007/s11094-005-0144-6.   DOI
9 Ghosh S, Jung C, Meyer-Rochow VB. Nutritional value and chemical composition of larvae, pupae, and adults of worker honey bee, Apis mellifera ligustica as a sustainable food source. J Asia Pac Entomol. 2016;19:487-95. https://doi.org/10.1016/j.aspen.2016.03.008.   DOI
10 De Groot AP. The influence of temperature and kind of food of the increase in the nitrogen content of the young worker honeybee (Apis mellifera L.). 45th communication of the "Werkgemeenschapvoor Endocrinologie", part of the National Council for Agricultural Research T.N.O. Proc K Akad Wet Ser C. 1950; Available from: https://www.dwc.knaw.nl/DL/publications/PU00018807.pdf, accessed 15th Sept. 2021.
11 Kim J-E, Kim D-I, Kim H-J, Kim S-Y, Lee Y-B, Moon J-H, et al. Characteristics of hydrolysis of protein in drone pupa (Apis mellifera L.). J Apiculture. 2020a; 35(3):169-77. https://doi.org/10.17519/apiculture.2020.09.35.3.169.   DOI
12 Paoli PP, Donley D, Stabler D, Saseendranath A, Nicolson SW, Simpson SJ, et al. Nutritional balance of essential amino acids and carbohydrates of the adult worker honeybee depends on age. Amino Acids. 2014;46:1449-58. https://doi.org/10.1007/s00726-014-1706-2.   DOI
13 Kipkoech C, Kinyuru JN, Imathiu S, Meyer-Rochow VB, Roos N. Invitro study of cricket chitosan's potential as a prebiotic and promoter of probiotic microorganisms to control pathogenic bacteria in the human gut. Foods. 2021;10(10):2310. https://doi.org/10.3390/foods10102310.   DOI
14 Meyer-Rochow VB, Gahukar RT, Ghosh S, Jung S. Chemical composition, nutrient quality and acceptability of edible insects are affected by species, developmental stage, gender, diet, and processing method. Foods. 2021;10:1036. https://doi.org/10.3390/foods10051036.   DOI
15 Micheu S, Crailsheim K, Leonhard B. Importance of proline and other amino acids during honeybee flight. Amino Acids. 2000;18:157-75. https://doi.org/10.1007/s007260050014.   DOI
16 Millward DJ, Fereday A, Gibson N, Pacy PJ. Aging, protein requirements, and protein turnover. Am J Clin Nutr. 1997;66(4):774-86. https://doi.org/10.1093/ajcn/66.4.774.   DOI
17 Roffet-Salque M, Regert M, Evershed RP, Outram AK, Cramp LJE, Decavallas O, et al. Widespread exploitation of the honeybee by early Neolithic farmers. Nature. 2015;527:226-30. https://doi.org/10.1038/nature15757.   DOI
18 Ghosh S, Herren P, Meyer-Rochow VB, Jung C. Nutritional composition of honey bee drones of two subspecies relative to their pupal developmental stages. Insects. 2021b;12(8):759. https://doi.org/10.3390/insects12080759.   DOI
19 Haydak MH. Changes with age in weight and nitrogen content of honeybees. Bee World. 1959;40(9):225-9. https://doi.org/10.1080/0005772X.1959.11096735.   DOI
20 Hollak CEM, van Weely S, van Oers MHJ, Aerts JM. Marked elevation of plasma chitotriosidase activity. A novel hallmark of Gaucher disease. J Clin Investig. 1994;93(3):1288-92. https://doi.org/10.1172/JCI117084.   DOI
21 Muzzarelli RAA, Boudrant J, Meyer D, Manno N, DeMarchis M, Paoletti MG. Current views on fungal chitin/chitosan, human chitinases, food preservation, glucans, pectins and inulin: a tribute to Henri Braconnot, precursor of the carbohydrate polymers science, on the chitin bicentennial. Carbohydr Polym. 2012;87(2):995-1012. https://doi.org/10.1016/j.carbpol.2011.09.063.   DOI
22 Hocking B. Bees knees. Proc Alta Entomol Soc. 1957;4:17.
23 Hocking B, Matsumura F. Bee brood as food. Bee World. 1960;41(5):113-20. https://doi.org/10.1080/0005772X.1960.11096777.   DOI
24 Arrese EL, Soulages JL. Insect fat body: energy, metabolism, and regulation. Annu Rev Entomol. 2010;55(1):207-25. https://doi.org/10.1146/annurev-ento-112408-085356.   DOI
25 Cherry RH. Use of insects by Australian Aborigines. Am Entomol. 1991;37(1):8-13. https://doi.org/10.1093/ae/37.1.8.   DOI
26 Draczynski Z. Honeybee corpses as an available source of chitin. J Appl Polym Sci. 2008;109(3):1974-81. https://doi.org/10.1002/app.28356.   DOI
27 Muraviev DW, Kalatzinskaja AM. Drone homogenate and hens productivity. Viestnik Kazanskovo GAU. 2014;1:132-4.
28 Murray SS, Schoeninger MJ, Bunn HT, Pickering TR, Marlett JA. Nutritional composition of some wild plant foods and honey used by Hazda foragers of Tanzania. J Food Compos Anal. 2001;14(1):3-13. https://doi.org/10.1006/jfca.2000.0960.   DOI
29 Nemtsev SV, Zueva OU, Khismatoullin RG, Khismatoullin MR, Varlamov VP. Bees as potential source of chitosan. Proceedings of the 37th International Apicultural Congress, 28 Oct-1 Nov 2001; Durban, South Africa. Available from: https://www.apimondia.com/docs/congress/2001/Papers/162.pdf accessed 24 Sep 2021.
30 Nemtsev SV, Zueva OY, Khismatullin MR, Albulov AI, Varlamov VP. Isolation of chitin and chitosan from honeybees. Appl Biochem Microbiol. 2004;40(1):39-43.   DOI
31 Ozimek L, Sauer WC, Kozikowski V, Ryan JK, Jorgensen H, Jelen P. Nutritive value of protein extracted from honey bees. J Food Sci. 1985;50(5):1327-9. https://doi.org/10.1111/j.1365-2621.1985.tb10469.x.   DOI
32 Lopez-Santamarina A, Mondragon AC, Lamas A, Miranda JM, Franco CM, Cepeda A. Animal-origin prebiotics based on Chitin: an alternative for the future? A critical review. Foods. 2020;9(6):782. https://doi.org/10.3390/foods9060782.   DOI
33 Kim SG, Woo SO, Bang KW, Jang HR, Han SM. Chemical composition of drone pupa of Apis mellifera and its nutritional evaluation. J Apiculture. 2018;33(1):17-23. https://doi.org/10.17519/apiculture.2018.04.33.1.17.   DOI
34 Kimura AH. Hidden hunger, gender and the politics of smarter foods. Ithaca, New York: Cornell University Press; 2013. p. 1-42.
35 Klein A-M, Vaissiere BE, Cane JH, Steffan-Dewenter I, Cunningham SA, Kremen C, et al. Importance of pollinators in changing landscapes for world crops. Proc R Soc B. 2007;274(1608):303-13. https://doi.org/10.1098/rspb.2006.3721.   DOI
36 Ruttner F. Biogeography and taxonomy of honeybees. Berlin, Germany: Springer-Verlag; 1988. p. 284p.
37 Seres AB, Ducza E, Bathori M, Hunyadi A, Beni Z, Dekany M, et al. 2013. Raw drone milk of honeybees elicits uterotrophic effects in rats: evidence for estrogenic activity. J Med Food. 2013;16(5):404-9. https://doi.org/10.1089/jmf.2012.0232.   DOI
38 Strauss J. Die chemische Zusammensetzung der Arbeitsbienen und Drohnen wahrend ihrer verschiedenen Entwicklungsstadien. Zoo Biol. 1911;56:347-97.
39 Vasilenko YK, Klimova OV, Lazaryan DS. Biological effect of drone brood under chronic hyperlipidemia conditions. Pharm Chem J. 2002;36:434-6. https://doi.org/10.1023/A:1021214728006.   DOI
40 Yucel B, Acikgoz Z, Bayraktar H, Seremet C. The effects of Apilarnil (drone bee larvae) administration on growth performance and secondary sex characteristics of male broilers. J Anim Vet Adv. 2011;10(17):2263-6.
41 Kim J-E, Kim D-I, Koo H-Y, Kim H-J, SOY K, Lee Y-B, et al. Analysis of nutritional compounds and antioxidant effect of freeze-dried powder of the honey bee (Apis mellifera L.) drone (pupal stage). Korean J Appl Entomol. 2020b;59(3):265-75. https://doi.org/10.5656/KSAE.2020.08.0.029.   DOI
42 Hu F, Li Y. Nutritive value and pharmacological actions of Italian worker bee larvae and pupae. Proceedings of the 37th International Apicultural Congress, Apimondia. Durban: Produced by: Document Transformation Technologies; 2001. ISBN: 0-620-27768-8. Available from: https://www.apimondia.com/docs/congress/2001/Papers/294.pdf. Accessed 2 Apr 2021.
43 Jensen AB, Evans J, Jonas-Levi A, Benjamin O, Martinez I, Dahle B, et al. Standard methods for Apis mellifera brood as human food. J Apicul Res. 2019;58(2):1-28. https://doi.org/10.1080/00218839.2016.1226606.   DOI
44 Kim J-E, Kim D-I, Koo H-Y, Kim H-J, Kim S-Y, Lee Y-B, et al. Evaluation of honey bee (Apis mellifera L.) drone pupa extracts on the improvement of hair loss. J Apiculture. 2020c;35(3):179-88. https://doi.org/10.17519/apiculture.2020.09.35.3.179.   DOI
45 Bamidele JA, Idowu AB, Ademolu K, Osipitan AA. Nutritional composition of Apis mellifera adansoniiL. (Hymenoptera: Apidae) from three ecological zones of Nigeria. J Apicul Res. 2021;60(3):445-56. https://doi.org/10.1080/00218839.2021.1874709.   DOI
46 Ghosh S, Chuttong B, Burgett M, Meyer-Rochow VB, Jung C. Nutritional value of brood and adult worker of the Asia honeybee species Apis cerana and Apis dorsata. In: Mariod AA, editor. In African edible insects as alternative source of food, oil, protein and bioactive components. Springer, Cham; 2020a. p. 265-73. https://doi.org/10.1007/978-3-030-32952-5_19.   DOI
47 Ghosh S, Jung C, Chuttong B, Burgett M. Nutritional aspects of the dwarf honeybee (Apsi florea F.) for human consumption. In: Abrol DP, editor. In The future role of dwarf honeybees in natural and agricultural systems. Boca Raton, FL: CRC Press; 2020b. p. 137-45.
48 Zhi-Yi L. Insects as food in China. Ecol Food Nutr. 1997;36(2-4):201-7. https://doi.org/10.1080/03670244.1997.9991515.   DOI
49 Ghosh S, Sohn H-Y, Pyo S-J, Jensen AB, Meyer-Rochow VB, Jung C. Nutritional composition of Apis mellifera drones from Korea and Denmark as a potential sustainable alternative food source: comparison between developmental stages. Foods. 2020c;9(4):389. https://doi.org/10.3390/foods9040389.   DOI
50 Haddad L. Women's status: levels, determinants, consequences for malnutrition, interventions, and policy. Asian Dev Rev. 1999;17(1-2):96-131.
51 Bolatovna KS, Rustenov A, Eleuqalieva N, Omirzak T, Akhanov UK. Improving reproductive qualities of pigs using the drone brood homogenate. Biol Med (Aligarh). 2015;7(2):2 3 BM-091-15.
52 Boot RG, Renkema GH, Verhoek M, Strijland A, Bliek J, de Meulemeester TM, et al. The human chitotriosidase gene. Nature of inherited enzyme deficiency. J Biol Chem. 1998;273(40):25680-5. https://doi.org/10.1074/jbc.273.40.25680.   DOI
53 FAO (Food and Agriculture Organization of the United Nations). Dietary protein quality evaluation in human nutrition. Rome, Italy: FAO; 2013.
54 Torre-Bueno JRD. Why not eat insects? Bull Brooklyn Entomol Soc. 1944;39:122-31.
55 Mbata KJ. Traditional use of arthropods in Zambia. I. The food insects. Food Insects Newsletter. 1995;8:5-7.
56 Ghosh S, Gahukar RT, Meyer-Rochow VB, Jung C. Future prospects of insects as biological resource in India: potential biological products utilizing insects with reference to the frontier countries. Entomoll Res. 2021a;51(5):209-29. https://doi.org/10.1111/1748-5967.12507.   DOI
57 Sawczuk R, Karpinska J, Miltyk W. What do we need to know about drone brood homogenate and what is known. J Ethnopharmacol. 2019;245:111581. https://doi.org/10.1016/j.jep.2018.10.042.   DOI
58 Shoinbayeva KB, Omirzak T, Bigara T, Abubakirova A, Dauylbay A. Biologically active preparation and reproductive function of stud rams. Asian J Pharm. 2017;11(3):184-91.
59 USDA Database on Nutrient Content of Food. Available online: http://www.data.nal.usda.gov accessed on 2 April 2021.
60 d'Errico F, Backwell L, Villa P, Degano I, Lucejko JJ, Bamford MK, et al. Early evidence of San material culture represented by organic artefacts from Border cave, South Africa. Proc Natl Acad Sci U S A. 2012;109(33):13214-9. https://doi.org/10.1073/pnas.1204213109.   DOI
61 Wongsiri S, Lekprayoon C, Thapa R, Thirakupt K, Rinderer TE, Sylvester HA, et al. Comparative biology of Apis andreniformis and Apis florea in Thailand. Bee World. 1997;78:23-35. https://doi.org/10.1080/0005772X.1997.11099328.   DOI
62 Paoletti MG, Norberto L, Damini R, Musumeci S. Human gastric juice contains chitinase that can degrade chitin. Ann Nutr Metab. 2007;51:244-51. https://doi.org/10.1159/000104144.   DOI
63 Paoletti MG, Norberto L, Cozzarini E, Musumeci S. Role of chitinase in human stomach for chitin digestion: AMCase in the gastric digestion of chitin and chitotrisidase in gastric pathologies. In: Musumeci S, Paoletti MG, editors. Binomium chitin-chitinase: Recent issues. New York: Nova Biomedical Books; 2009.