Register      Login
Animal Production Science Animal Production Science Society
Food, fibre and pharmaceuticals from animals
RESEARCH ARTICLE

Nutritional evaluation of dried larvae and pupae meal of the housefly (Musca domestica) using chemical- and broiler-based biological assays

E. Pieterse A B and Q. Pretorius A
+ Author Affiliations
- Author Affiliations

A Department of Animal Sciences, Stellenbosch University, Private bag X1, Matieland 7602, South Africa.

B Corresponding author. Email: elsjep@sun.ac.za

Animal Production Science 54(3) 347-355 https://doi.org/10.1071/AN12370
Submitted: 23 October 2012  Accepted: 11 March 2013   Published: 28 May 2013

Abstract

The nutritional composition of common housefly (Musca domestica) larvae and pupae meal is reported in terms of proximate analysis, amino acid profile, fatty acid composition, apparent metabolisable energy and total tract digestibility (TTD) of nutrients. Proximate analysis and TTD of meal showed larvae and pupae meal to contain, on a DM basis, a gross energy value of 20.10 MJ/kg and 20.42 MJ/kg, respectively, and an apparent metabolisable energy value of 14.23 MJ/kg and 15.15 MJ/kg, respectively. Crude protein content was 60.38% and 76.23%, with TTDs of 69% and 79%, respectively, with similarly high values reported for individual amino acids. Amino acid analysis revealed a favourable amino acid composition with high lysine concentrations but marginally low methionine concentrations. Arginine : lysine ratios of larvae and pupae meal were 0.67 and 0.91, respectively, and isoleucine : leucine ratios were 0.68 and 0.64, respectively. Crude fat contents were 14.08% and 14.39%, with TTDs of 94% and 98%, respectively, and crude fibre contents were 8.59% and 15.71%, with TTDs of 62% and 58%. Housefly larvae meal had crude protein TTD of 69%, whereas that of pupae meal was 79%. Both larvae and pupae meal had high amino acid TTDs. The TTD values of the crude fat and crude fibre were determined at 94% and 62%, respectively, for the housefly larvae, and at 98% and 58%, respectively, for the housefly pupae. M. domestica larvae meal can therefore be regarded as a good-quality protein source suitable for animal feeding.

Additional keywords: magmeal, total tract digestibility.


References

AgriLASA (2007) Method no. 6.1.1 for feeds and plants. In ‘Agrilasa Handbook of Feeds and Plant Analysis. Vol. 1’. 2nd edn. (Eds P Palic, AS Claasens, J Collier, A Loock, D Hattingh) (Agri Laboratory Association of South Africa: Pretoria)

Ai H, Wang F, Yang Q, Zhu F, Lei C (2008) Preparation and biological activities of chitosan from the larvae of housefly, Musca domestica. Carbohydrate Polymers 72, 419–423.
Preparation and biological activities of chitosan from the larvae of housefly, Musca domestica.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1cXislWmsrg%3D&md5=b5f1d269b70432aa247bc5f292ab3e56CAS |

Aksnes A, Hjertnes T, Opstvedt J (1996) Comparison of two assay methods for determination of nutrient and energy digestibility in fish. Aquaculture 140, 343–359.
Comparison of two assay methods for determination of nutrient and energy digestibility in fish.Crossref | GoogleScholarGoogle Scholar |

Aniebo AO, Erondu ES (2008) Performance of varying blends of wheat bran and saw dust as absorbent materials for blood waste in commercial maggotry. International Journal of Biotechnology & Biochemistry May, 1–6.

Aniebo AO, Owen OJ (2010) Effects of age and method of drying on the proximate composition of housefly larvae (Musca domestica Linnaeus) meal (HFLM). Pakistan Journal of Nutrition 9, 485–487.
Effects of age and method of drying on the proximate composition of housefly larvae (Musca domestica Linnaeus) meal (HFLM).Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3cXlvF2ksLY%3D&md5=86733cf5ea5fe2552edb2d30350fa8ecCAS |

Aniebo AO, Erondu ES, Owen OJ (2008) Proximate composition of housefly larvae (Musca domestica) meal generated from mixture of cattle blood and wheat bran. Livestock Research for Rural Development 20, 1–2.

Association of Official Analytical Chemists International (AOAC) (2002) ‘Official methods of analysis of AOAC international.’ (Association of Official Analytical Chemists International: Arlington, VA)

Atteh JO, Ologbenla FD (1993) Replacement of fish meal with maggots in broiler diets. Effects on performance and nutrient retention. Nigerian Journal of Animal Production 20, 44–49.

Austic RE, Nesheim MC (1970) Role of kidney arginase in variations of the arginine requirement of chicks. The Journal of Nutrition 100, 855–867.

Austic RE, Scott RL (1975) Involvement of food intake in the lysine–arginine antagonism in chicks. The Journal of Nutrition 105, 1122–1131.

Avery S, Moore A, Hutchison M (2004) Fate of Escherichia coli originating from livestock faeces deposited directly onto pasture. Letters in Applied Microbiology 38, 355–359.
Fate of Escherichia coli originating from livestock faeces deposited directly onto pasture.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DC%2BD2c7ms1Citw%3D%3D&md5=ef9e92c624b01e69f276f90c13b5fd07CAS | 15059203PubMed |

Awoniyi TAM, Aletor VA, Aina JM (2003) Performance of broiler-chickens fed on maggot meal in place of fishmeal. International Journal of Poultry Science 2, 271–274.
Performance of broiler-chickens fed on maggot meal in place of fishmeal.Crossref | GoogleScholarGoogle Scholar |

Awoniyi TAM, Adebayo IA, Aletor VA (2004a) A study of some erythrocyte indices and bacteriological analysis of broiler-chickens raised on maggot-meal based diets. International Journal of Poultry Science 3, 386–390.
A study of some erythrocyte indices and bacteriological analysis of broiler-chickens raised on maggot-meal based diets.Crossref | GoogleScholarGoogle Scholar |

Awoniyi TAM, Adetuyi FC, Akinyosoye FA (2004b) Microbiological investigation of maggot meal, stored for use as livestock feed component. Journal of Food Agriculture and Environment 2, 104–106.

Burnham D, Gous RM (1992) Isoleucine requirements of the chicken: requirement for maintenance. British Poultry Science 33, 59–69.
Isoleucine requirements of the chicken: requirement for maintenance.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK38XksVOiu7c%3D&md5=e6ca7f1c9646755207f8749a1ce4de57CAS | 1571808PubMed |

Calvert CC, Martin RD, Morgan NO (1969) House fly pupae as food for poultry. Journal of Economic Entomology 62, 938–939.

Cobb International (2008) Cobb broiler management guide. Available at http://www.cobb-vantress.com/products/guide-library/general/broiler-management-guide [verified 24 April 2013]

Crespo N, Esteve-Garcia E (2002) Dietary polyunsaturated fatty acids decrease fat deposition in separable fat depots but not in the remainder carcass. Poultry Science 81, 512–518.

Cunico R, Mayer AG, Wehr CT, Sheehan TL (1986) High sensitivity amino acid analysis using a novel automated precolumn derivatization system. Biochromatography 1, 6–14.

Daeschlein G, Mumcuoglu KY, Assadian O, Hoffmeister B, Kramer A (2007) In vitro antibacterial activity of Lucilia sericata maggot secretions. Skin Pharmacology and Physiology 20, 112
In vitro antibacterial activity of Lucilia sericata maggot secretions.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DC%2BD2s7ksFCjsA%3D%3D&md5=d33d7acac48a4f8801505fcfd5043affCAS | 17167275PubMed |

Dolk H, Vrijheid M, Armstrong B, Abramsky L, Bianchi F, Garne E, Nelen V, Robert E, Scott JES, Stone D (1998) Risk of congenital anomalies near hazardous-waste landfill sites in Europe: the EUROHAZCON study. Lancet 352, 423–427.
Risk of congenital anomalies near hazardous-waste landfill sites in Europe: the EUROHAZCON study.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DyaK1cznt1Crsg%3D%3D&md5=d9ed2d0de198688e29733c0f11e58fb1CAS | 9708749PubMed |

El-Fadel M, Findikakis AN, Leckie JO (1997) Environmental impacts of solid waste landfilling. Journal of Environmental Management 50, 1–25.
Environmental impacts of solid waste landfilling.Crossref | GoogleScholarGoogle Scholar |

Erickson MC, Islam M, Sheppard C, Liao J, Doyle MP (2004) Reduction of Escherichia coli O157: H7 and Salmonella enterica serovar enteritidis in chicken manure by larvae of the black soldier fly. Journal of Food Protection 174, 685–690.

Fasakin EA, Balogun AM, Ajayi OO (2003) Evaluation of full-fat and defatted maggot meals in the feeding of clariid catfish Clarias gariepinus fingerlings. Aquaculture and Research 34, 733–738.
Evaluation of full-fat and defatted maggot meals in the feeding of clariid catfish Clarias gariepinus fingerlings.Crossref | GoogleScholarGoogle Scholar |

Fox T (2013) ‘Global food, waste not, want not. January 2013.’ (Institution of Mechanical Engineers). Available at http://www.imeche.org/knowledge/themes/environment/global-food [verified 5 April 2013]

Freeman CP (1983) Fat supplementation in animal production – monogastric animals. The Proceedings of the Nutrition Society 42, 351–359.
Fat supplementation in animal production – monogastric animals.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DyaL3szgtVWnsA%3D%3D&md5=20964670c1068e28e62ad8695b21e157CAS | 6351090PubMed |

Gong X, Le GW, Li YF (2005) Antibacterial spectrum of antibacterial peptides from Musca domestica larvae and synergic interaction between the peptides and antibiotics. Acta Microbiologica Sinica 45, 516–520.

Guo GUO, Jian-wei WU, Ping FU (2008) Effect of musca domestica larvae secretion from different sources on development of ascaris suum egg. Chinese Journal of Public Health 1, 30–35.

Harbin LJ, Khan M, Thompson EM, Goldin RD (2002) A sebaceous cyst with a difference: Dermatobia hominis. Journal of Clinical Pathology 55, 798–799.
A sebaceous cyst with a difference: Dermatobia hominis.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DC%2BD38vptlCitw%3D%3D&md5=d8be81d744c5b60770e9275f9ee6daa2CAS | 12354816PubMed |

Hou L, Shi Y, Zhai P, Le G (2007) Antibacterial activity and in vitro anti-tumor activity of the extract of the larvae of the housefly (Musca domestica). Journal of Ethnopharmacology 111, 227–231.
Antibacterial activity and in vitro anti-tumor activity of the extract of the larvae of the housefly (Musca domestica).Crossref | GoogleScholarGoogle Scholar | 17227700PubMed |

Hwangbo J, Hong EC, Jang A, Kang HK, Oh JS, Kim BW, Park BS (2009) Utilization of house fly-maggots, a feed supplement in the production of broiler chickens. Journal of Environmental Biology 30, 609–614.

Inaoka T, Okubo G, Yokota M, Takemasa M (1999) Nutritive value of house fly larvae and pupae fed on chicken feces as food source for poultry. Japanese Poultry Science 36, 174–180.
Nutritive value of house fly larvae and pupae fed on chicken feces as food source for poultry.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK1MXjslait78%3D&md5=7f3e84e0d57a66c4a96ec09d507d03d4CAS |

Jones JD, Wolters R, Burnett PC (1966) Lysine–arginine-electrolyte relationships in the rat. The Journal of Nutrition 89, 171–188.

Kovacs MIP, Anderson WE, Ackman RG (1979) A simple method for the determination of cholesterol and some plant sterols in fishery-based food products. Journal of Food Science 44, 1299–1301.
A simple method for the determination of cholesterol and some plant sterols in fishery-based food products.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaE1MXlvFWntr0%3D&md5=7eeb8ad72fbd0ee7940f0407dcfc8d51CAS |

Lam K, Thu K, Tsang M, Moore M, Gries G (2009) Bacteria on housefly eggs, Musca domestica, suppress fungal growth in chicken manure through nutrient depletion or antifungal metabolites. Naturwissenschaften 96, 1127–1132.
Bacteria on housefly eggs, Musca domestica, suppress fungal growth in chicken manure through nutrient depletion or antifungal metabolites.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1MXpvFaqsb4%3D&md5=98fc88d210bfb9b754866b8b23f467e8CAS | 19636523PubMed |

Leeson S, Summers JD (2005) ‘Commercial poultry nutrition.’ (University Books Ontario: Guelph, Ontario, Canada).

Lerch K, Linde H, Lehn N, Grifka J (2003) Bacteria ingestion by blowfly larvae: an in vitro study. Dermatology 207, 362–366.
Bacteria ingestion by blowfly larvae: an in vitro study.Crossref | GoogleScholarGoogle Scholar | 14657627PubMed |

Levinson ZH, Silverman PH (1954) Studies on the lipids of Musca vicina (Macq.) during growth and metamorphosis. Biochemical Journal 58, 294–296.

Lindner P (1919) Extraction of fat from small animals. Zootechnica Biologica 7, 213–220.

Liu Q, Tomberlin JK, Brady JA, Sanford MR, Yu Z (2008) Black soldier fly (Diptera: Stratiomyidae) larvae reduce Escherichia coli in dairy manure. Environmental Entomology 37, 1525–1530.
Black soldier fly (Diptera: Stratiomyidae) larvae reduce Escherichia coli in dairy manure.Crossref | GoogleScholarGoogle Scholar | 19161696PubMed |

Ludwig D, Crowe PA, Hassemer MM (1964) Free fat and glycogen during metamorphosis of Musca domestica L. Journal of the New York Entomological Society 72, 23–28.

McDonald P (2002) ‘Animal nutrition.’ (Prentice Hall: Harlow, UK)

NRC (1977) ‘Nutrient requirements of poultry.’ National Research Council (US) Subcommittee on Poultry Nutrition. (National Academy of Sciences: Washington, DC)

Nazni WA, Seleena B, Lee HL, Jeffery J, Rogayah TA, Sofian MA (2005) Bacteria fauna from the house fly, Musca domestica (L.). Tropical Biomedicine 22, 225–231.

Newton GL, Booram CV, Barker RW, Hale OM (1977) Dried Hermetia illucens larvae meal as a supplement for swine. Journal of Animal Science 44, 395–400.

Newton L, Sheppard C, Watson DW, Burtle G, Dove R (2005) Using the black soldier fly, Hermetia illucens, as a value-added tool for the management of swine manure. Animal and Poultry Waste Management Center, North Carolina State University, Raleigh, NC.

Nzamujo OP (1999) Technique for maggot production – The Songhai Experience. Available at http://www.ias.unu.edu/proceedings/icibs/ibs/songhai/index.htm [verified 13 April 2010]

Ogunji JO, Kloas W, Wirth M, Schulz W, Rennert B (2008) Housefly maggot meal (Magmeal) as a protein source for Oreochromis niloticus (Linn.). Asian Fisheries Science 20, 319–331.

Omogbenigun FO, Nyachoti CM, Slominski BA (2004) Dietary supplementation with multienzyme preparations improves nutrient utilization and growth performance in weaned pigs. Journal of Animal Science 82, 1053–1061.

Parsons CM (1996) Digestible amino acids for poultry and swine. Animal Feed Science and Technology 59, 147–153.
Digestible amino acids for poultry and swine.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK28XksFSnu74%3D&md5=11e725a0c4c7ce324dae32c9b40179fdCAS |

Pearincott JV (1960) Changes in the lipid content during growth and metamorphosis of the house fly, Musca domestica Linnaeus. Journal of Cellular and Comparative Physiology 55, 167–174.
Changes in the lipid content during growth and metamorphosis of the house fly, Musca domestica Linnaeus.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaF3MXpsl2n&md5=d41b6299f72cba6a67ab43ab7fcb108cCAS | 13733761PubMed |

Qu J, Chen P, Qu X, Li W, Tang B, Huang T (2005) Purification and biological activities of novel antibacterial peptides from Musca domestica. Electronic Journal of Biology 1, 49–55.

Resh VH, Cardé RT (2003) ‘Encyclopedia of insects.’ (Academic Press: Amsterdam)

Scholtz CH, Holm E (1986) ‘Insects of southern Africa.’ (Butterworths: Durban)

Scott TA, Boldaji F (1997) Comparison of inert markers [chromic oxide or insoluble ash (Celite)] for determining apparent metabolizable energy of wheat-or barley-based broiler diets with or without enzymes. Poultry Science 76, 594–598.

Scott TA, Hall JW (1998) Using acid insoluble ash marker ratios (diet: digesta) to predict digestibility of wheat and barley metabolizable energy and nitrogen retention in broiler chicks. Poultry Science 77, 674–679.

Sebastian S, Touchburn SP, Chavez ER, Lague PC (1997) Apparent digestibility of protein and amino acids in broiler chickens fed a corn–soybean diet supplemented with microbial phytase. Poultry Science 76, 1760–1769.

Sehgal R, Bhatti HP, Bhasin DK, Sood AK, Nada R, Malla N, Singh K (2002) Intestinal myiasis due to Musca domestica: a report of two cases. Japanese Journal of Infectious Diseases 55, 191–193.

Sheppard DC, Newton GL, Burtle G (2007) Black soldier fly prepupae. A compelling alternative to fish meal and fish oil. Available at http://www.extension.org/pages/15054/research-summary:-black-soldier-fly-prepupae-a-compelling-alternative-to-fish-meal-and-fish-oil [verified 24 April 2013]

Shimomura Y, Tamura T, Suzuki M (1990) Less body fat accumulation in rats fed a safflower oil diet than in rats fed a beef tallow diet. The Journal of Nutrition 120, 1291–1296.

St‐Hilaire S, Sheppard C, Tomberlin JK, Irving S, Newton L, McGuire MA, Mosley EE, Hardy RW, Sealey W (2007) Fly prepupae as a feedstuff for rainbow trout, Oncorhynchus mykiss. Journal of the World Aquaculture Society 38, 59–67.
Fly prepupae as a feedstuff for rainbow trout, Oncorhynchus mykiss.Crossref | GoogleScholarGoogle Scholar |

Teguia A, Beynen AC (2005) Alternative feedstuffs for broilers in Cameroon. Livestock Research for Rural Development 17, Article#34

Teotia JS, Miller BF (1974) Nutritive content of house fly pupae and manure residue. British Poultry Science 15, 177–182.
Nutritive content of house fly pupae and manure residue.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaE2cXks1antLc%3D&md5=ccfdd44317a807415eaaf00a83ff9944CAS |

Turunen S (1973) Role of labelled dietary fatty acids and acetate in phospholipids during the metamorphosis of Pieris brassicae. Journal of Insect Physiology 19, 2327–2340.
Role of labelled dietary fatty acids and acetate in phospholipids during the metamorphosis of Pieris brassicae.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaE2cXjsFejsg%3D%3D&md5=1a10bd6f3c34e16b72a743802432f8c8CAS |

van der Plas M, Jukema G, Wai S, Dogterom-Ballering H, Lagendijk E, Van Gulpen C, Van Dissel J, Bloemberg G, Nibbering P (2008) Maggot excretions/secretions are differentially effective against biofilms of Staphylococcus aureus and Pseudomonas aeruginosa. The Journal of Antimicrobial Chemotherapy 61, 117–122.
Maggot excretions/secretions are differentially effective against biofilms of Staphylococcus aureus and Pseudomonas aeruginosa.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1cXhtFWmtw%3D%3D&md5=64c029b953db0c4f058e946f99f87967CAS | 17965032PubMed |

Van Jaarsveld PJ, Smuts HY, Tichelaar M, Kruger AJ, Spinnler Benadé P (2000) Effect of palm oil on plasma lipoprotein concentrations and plasma low-density lipoprotein composition in non-human primates. International Journal of Food Sciences and Nutrition 51, S21–S30.
Effect of palm oil on plasma lipoprotein concentrations and plasma low-density lipoprotein composition in non-human primates.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3MXkvF2ksQ%3D%3D&md5=26e87296cf06c8b874bd28cbb5173edcCAS | 11271853PubMed |

Van Keulen J, Young BA (1977) Evaluation of acid-insoluble ash as a natural marker in ruminant digestibility studies. Journal of Animal Science 44, 282–287.

Wenk C (2001) The role of dietary fibre in the digestive physiology of the pig. Animal Feed Science and Technology 90, 21–33.
The role of dietary fibre in the digestive physiology of the pig.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3MXislGmtbk%3D&md5=ff978e974adb797eaa69e6c6863d8423CAS |

Yamamoto T, Yasuhara A, Shiraishi H, Nakasugi O (2001) Bisphenol A in hazardous waste landfill leachates. Chemosphere 42, 415–418.
Bisphenol A in hazardous waste landfill leachates.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3cXoslOqu70%3D&md5=eeaf8ebf325ddbfbc7d24e42b551aa28CAS | 11100793PubMed |

Yu G (2011) Inoculating poultry manure with companion bacteria influences growth and development of black soldier fly (Diptera: Stratiomyidae) larvae. Environmental Entomology 40, 30–35.
Inoculating poultry manure with companion bacteria influences growth and development of black soldier fly (Diptera: Stratiomyidae) larvae.Crossref | GoogleScholarGoogle Scholar | 22182608PubMed |

Zuidhof MJ, Molnar CL, Morley FM, Wray TL, Robinson FE, Khan BA, Al-Ani L, Goonewardene LA (2003) Nutritive value of house fly (Musca domestica) larvae as a feed supplement for turkey poults. Animal Feed Science and Technology 105, 225–230.
Nutritive value of house fly (Musca domestica) larvae as a feed supplement for turkey poults.Crossref | GoogleScholarGoogle Scholar |