Hostname: page-component-78c5997874-xbtfd Total loading time: 0 Render date: 2024-11-05T08:30:31.344Z Has data issue: false hasContentIssue false
  • English
  • Français

Yellow mealworm (Tenebrio molitor L.) larvae inclusion in diets for free-range chickens: effects on meat quality and fatty acid profile

Published online by Cambridge University Press:  09 May 2019

S. Dabbou Open the ORCID record for S. Dabbou [Opens in a new window] ,
L. Gasco Open the ORCID record for L. Gasco [Opens in a new window] ,
C. Lussiana Open the ORCID record for C. Lussiana [Opens in a new window] ,
A. Brugiapaglia Open the ORCID record for A. Brugiapaglia [Opens in a new window] ,
I. Biasato Open the ORCID record for I. Biasato [Opens in a new window] ,
M. Renna Open the ORCID record for M. Renna [Opens in a new window] ,
L. Cavallarin Open the ORCID record for L. Cavallarin [Opens in a new window] ,
F. Gai Open the ORCID record for F. Gai [Opens in a new window]  and
A. Schiavone Open the ORCID record for A. Schiavone [Opens in a new window]
S. Dabbou
Affiliation:
Department of Veterinary Science, University of Turin, largo Paolo Braccini 2, 10095 Grugliasco, Turin, Italy
L. Gasco*
Affiliation:
Department of Agricultural, Forest and Food Sciences, University of Turin, largo Paolo Braccini 2, 10095 Grugliasco, Turin, Italy Institute of Science of Food Production, National Research Council, largo Paolo Braccini 2, 10095 Grugliasco, Turin, Italy
C. Lussiana
Affiliation:
Department of Agricultural, Forest and Food Sciences, University of Turin, largo Paolo Braccini 2, 10095 Grugliasco, Turin, Italy
A. Brugiapaglia
Affiliation:
Department of Agricultural, Forest and Food Sciences, University of Turin, largo Paolo Braccini 2, 10095 Grugliasco, Turin, Italy
I. Biasato
Affiliation:
Department of Agricultural, Forest and Food Sciences, University of Turin, largo Paolo Braccini 2, 10095 Grugliasco, Turin, Italy
M. Renna
Affiliation:
Department of Veterinary Science, University of Turin, largo Paolo Braccini 2, 10095 Grugliasco, Turin, Italy
L. Cavallarin
Affiliation:
Institute of Science of Food Production, National Research Council, largo Paolo Braccini 2, 10095 Grugliasco, Turin, Italy
F. Gai
Affiliation:
Institute of Science of Food Production, National Research Council, largo Paolo Braccini 2, 10095 Grugliasco, Turin, Italy
A. Schiavone
Affiliation:
Department of Veterinary Science, University of Turin, largo Paolo Braccini 2, 10095 Grugliasco, Turin, Italy Institute of Science of Food Production, National Research Council, largo Paolo Braccini 2, 10095 Grugliasco, Turin, Italy Institute of Interdisciplinary Research on Sustainability, University of Turin, Via Accademia Albertina 13, 10123, Turin, Italy
*
Author for correspondence: L. Gasco, E-mail: [email protected]
Get access Rights & Permissions [Opens in a new window]

Abstract

This study evaluated the effects of a diet containing yellow mealworm (Tenebrio molitor L.; TM) larva meal on quality parameters (pH24, color and drip losses), proximate composition and fatty acid (FA) profile of meat from free-range chickens. A total of 140 medium-growing hybrid female chickens were free-range reared and randomly allotted to two dietary treatments: a control group and a TM group, in which TM meal was included at 75 g kg−1 as fed in substitution of corn gluten meal. Each group consisted of five pens as replicates, with 14 chicks per pen. At 97 days of age, ten birds (two birds/pen) from each feeding group were slaughtered at a commercial abattoir. Quality parameters and proximate composition of breast and thigh meat were not affected by treatment. The effects of dietary TM larva meal on the FA profile of thigh meat were negligible. Breast meat from TM-fed chickens showed higher oleic and α-linolenic acid percentages as well as lower atherogenicity and thrombogenicity indexes. In conclusion, this study demonstrated that TM inclusion in diets for free-range chickens did not prejudice meat quality traits. The obtained results confirm that TM can be considered a promising insect protein source for the poultry feed industry.

Keywords

Breastfatty acidsfree-range chickensTenebrio molitor larva mealthigh
Type
Research Paper
Information
Renewable Agriculture and Food Systems , Volume 35 , Issue 5 , October 2020 , pp. 571 - 578
Check for updates
Copyright
Copyright © Cambridge University Press 2019

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

References

Alves, SP, Cabrita, ARJ, Fonseca, AJM and Bessa, RJB (2008) Improved method for fatty acid analysis in herbage based on direct transesterification followed by solid-phase extraction. Journal of Chromatography A 1209, 212–219.CrossRefGoogle ScholarPubMed
AOAC International (2000) Official Methods of Analysis, 17th Edn. Gaithersburg, MD, USA: Association of Official Analytical Chemists.Google Scholar
AOAC International (2003) Official Methods of Analysis, 17th Edn, 2nd revision. Gaithersburg, MD, USA: Association of Official Analytical Chemists.Google Scholar
AOAC International (2005) Official Methods of Analysis, 18th Edn. Washington, DC, USA: Association of Official Analytical Chemists.Google Scholar
Ballitoc, DA 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 e23050425. http://doi.org/10.7392/openaccess.23050425.Google Scholar
Belforti, M, Gai, F, Lussiana, C, Renna, M, Malfatto, V, Rotolo, L, De Marco, M, Dabbou, S, Schiavone, A, Zoccarato, I and Gasco, L (2015) Tenebrio molitor meal in rainbow trout (Oncorhynchus mykiss) diets: effects on animal performance, nutrient digestibility and chemical composition of fillets. Italian Journal of Animal Science 14, 670–676.CrossRefGoogle Scholar
Biasato, I, De Marco, M, Rotolo, L, Renna, M, Dabbou, S, Capucchio, MT, Biasibetti, E, Tarantola, M, Costa, P, Gai, F, Pozzo, L, Dezzutto, D, Bergagna, S, Gasco, L and Schiavone, A (2016) Effects of dietary Tenebrio molitor meal inclusion in free-range chickens. Journal of Animal Physiology and Animal Nutrition 100, 1104–1112.CrossRefGoogle ScholarPubMed
Biasato, I, Gasco, L, De Marco, M, Renna, M, Rotolo, L, Dabbou, S, Capucchio, MT, Biasibetti, E, Tarantola, M, Bianchi, C, Cavallarin, L, Gai, F, Pozzo, L, Dezzutto, D, Bergagna, S and Schiavone, A (2017) Effects of yellow mealworm larvae (Tenebrio molitor) inclusion in diets for female broiler chickens: implications for animal health and gut histology. Animal Feed Science and Technology 234, 253–263.CrossRefGoogle Scholar
Biasato, I, Gasco, L, De Marco, M, Renna, M, Rotolo, L, Dabbou, S, Capucchio, MT, Biasibetti, E, Tarantola, M, Sterpone, L, Cavallarin, L, Gai, F, Pozzo, L, Bergagna, S, Dezzutto, D, Zoccarato, I and Schiavone, A (2018) Yellow mealworm larvae (Tenebrio molitor) inclusion in diets for male broiler chickens: effects on growth performance, gut morphology and histological findings. Poultry Science 97, 540–548.CrossRefGoogle ScholarPubMed
Bovera, F, Piccolo, G, Gasco, L, Marono, S, Loponte, R, Vassalotti, G, Mastellone, V, Lombardi, P, Attia, YA and Nizza, A (2015) Yellow mealworm larvae (Tenebrio molitor, L.) as a possible alternative to soybean meal in broiler diets. British Poultry Science 56, 569–575.Google ScholarPubMed
Bovera, F, Loponte, R, Marono, S, Piccolo, G, Parisi, G, Iaconisi, V, Gasco, L and Nizza, A (2016) Use of Tenebrio molitor larvae meal as protein source in broiler diet: effect on growth performance, nutrient digestibility, and carcass and meat traits. Journal of Animal Science 94, 639–647.CrossRefGoogle Scholar
Castellini, C, Mugnai, C and Dal Bosco, A (2002) Effect of organic production system on broiler carcass and meat quality. Meat Science 60, 219–225.CrossRefGoogle ScholarPubMed
Commission Internationale de l’Éclairage (1976) Recommendations on Uniform Colour Spaces-Colour Difference Equations, Psychometric Colour Terms (Supplement no. 2 to CIE Publication No. 15). Paris, France: Commission Internationale de l’Éclairage.Google Scholar
Cullere, M, Tasoniero, G, Giaccone, V, Miotti-Scapin, R, Claeys, E, De Smet, S and Dalle Zotte, A (2016) Black soldier fly as dietary protein source for broiler quails: apparent digestibility, excreta microbial load, feed choice, performance, carcass and meat traits. Animal: An International Journal of Animal Bioscience 10, 1923–1930.CrossRefGoogle ScholarPubMed
Cullere, M, Tasoniero, G, Giaccone, V, Acuti, G, Marangon, A and Dalle Zotte, A (2018) Black soldier fly as dietary protein source for broiler quails: meat proximate composition, fatty acid and amino acid profile, oxidative status and sensory traits. Animal: An International Journal of Animal Bioscience 12, 640–647.CrossRefGoogle ScholarPubMed
Dal Bosco, A, Mugnai, C, Rosati, A, Paoletti, A, Caporali, S and Castellini, C (2014) Effect of range enrichment on performance, behavior and forage intake of free-range chickens. Journal of Applied Poultry Research 23, 137–145.CrossRefGoogle Scholar
De Marco, M, Martínez, S, Hernandez, F, Madrid, J, Gai, F, Rotolo, L, Belforti, M, Bergero, D, Katz, H, Dabbou, S, Kovitvadhi, A, Zoccarato, I, Gasco, L and Schiavone, A (2015) Nutritional value of two insect meals (Tenebrio molitor and Hermetia illucens) for broiler chickens: apparent nutrient digestibility, apparent ileal amino acid digestibility and apparent metabolizable energy. Animal Feed Science and Technology 209, 211–218.CrossRefGoogle Scholar
Fanatico, AC (2006) Alternative Poultry Production Systems and Outdoor Access. NCAT Agriculture Specialist: ATTRA Publications, Butte, Montana, (24p). Available at http://www.attra.ncat.org/attra-pub/poultry_access.pdf.Google Scholar
Fanatico, AC, Cavitt, LC, Pillai, PB, Emmert, JL and Owens, CM (2005) Evaluation of slow-growing broiler genotypes grown with and without outdoor access: meat quality. Poultry Science 84, 1785–1790.CrossRefGoogle ScholarPubMed
Fanatico, AC, Pillai, PB, Emmert, JL and Owens, CM (2007) Meat quality of slow- and fast-growing chicken genotypes fed low-nutrient or standard diets and raised indoors or with outdoor access. Poultry Science 86, 2245–2255.CrossRefGoogle ScholarPubMed
Fletcher, DL, Qiao, M and Smith, MP (2000) The relationship of raw broiler breast meat color and pH to cooked meat color and pH. Poultry Science 79, 784–788.CrossRefGoogle ScholarPubMed
Gasco, L, Henry, M, Piccolo, G, Marono, S, Gai, F, Renna, M, Lussiana, C, Antonopoulou, E, Mola, P and Chatzifotis, S (2016) Tenebrio molitor meal in diets for European sea bass (Dicentrarchus labrax L.) juveniles: growth performance, whole body composition and in vivo apparent digestibility. Animal Feed Science and Technology 220, 34–45.CrossRefGoogle Scholar
Gasco, L, Gai, F, Maricchiolo, G, Genovese, L, Ragonese, S, Bottari, T and Caruso, G (2018) Fishmeal alternative protein sources for aquaculture feeds. In Gasco, L, Gai, F, Maricchiolo, G, Genovese, L, Ragonese, S, Bottari, T and Caruso, G (eds). Feeds for the Aquaculture Sector – Current Situation and Alternative Sources. SpringerBriefs in Molecular Science. Cham: Springer, pp. 1–20. https://link.springer.com/chapter/10.1007/978-3-319-77941-6_1.Google Scholar
Honikel, KO (1998) Reference methods for the assessment of physical characteristics of meat. Meat Science 49, 447–457.CrossRefGoogle ScholarPubMed
Hussain, I, Khan, S, Sultan, A, Chand, N, Khan, R, Alam, W and Ahmad, N (2017) Meal worm (Tenebrio molitor) as potential alternative source of protein supplementation in broiler. International Journal of Bioscience 10, 255–262.Google Scholar
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 (Pagellus bogaraveo). Aquaculture 476, 49–58.CrossRefGoogle Scholar
Janssen, RH, Vincken, JP, van den Broek, LAM, Fogliano, V and Lakemond, CMM (2017) Nitrogen-to-protein conversion factors for three edible insects: Tenebrio molitor, Alphitobius diaperinus, and Hermetia illucens. Journal of Agricultural and Food Chemistry 65, 2275–2278.CrossRefGoogle ScholarPubMed
Kierończyk, B, Rawski, M, Józefiak, A, Mazurkiewicz, J, Świątkiewicz, S, Siwek, M, Bednarczyk, M, Szumacher-Strabel, M, Cieślak, A, Benzertiha, A and Józefiak, D (2018) Effects of replacing soybean oil with selected insect fats on broilers. Animal Feed Science and Technology 240, 170–183.CrossRefGoogle Scholar
Lands, B (2014) Historical perspectives on the impact of n-3 and n-6 nutrients on health. Progress in Lipid Research 55, 17–29.CrossRefGoogle ScholarPubMed
Lazzaroni, C, Biagini, D and Lussiana, C (2009) Fatty acid composition of meat and perirenal fat in rabbits from two different rearing systems. Meat Science 83, 135–139.CrossRefGoogle ScholarPubMed
Leiber, F, Gelencsér, T, Stamer, A, Amsler, Z, Wohlfahrt, J, Früh, B and Maurer, V (2017) Insect and legume-based protein sources to replace soybean cake in an organic broiler diet: effects on growth performance and physical meat quality. Renewable Agriculture and Food Systems 32, 21–27.CrossRefGoogle Scholar
Loponte, R, Nizza, S, Bovera, F, De Riu, N, Fliegerova, K, Lombardi, P, Vassalotti, G, Mastellone, V, Nizza, A and Moniello, G (2017) Growth performance, blood profiles and carcass traits of Barbary partridge (Alectoris barbara) fed two different insect larvae meals (Tenebrio molitor and Hermetia illucens). Research in Veterinary Science 115, 183–188.CrossRefGoogle Scholar
Loponte, R, Bovera, F, Piccolo, G, Gasco, L, Secci, G, Iaconisi, V and Parisi, G (2019) Fatty acid profile of lipids and caeca volatile fatty acid production of broilers fed a full fat meal from Tenebrio molitor larvae. Italian Journal of Animal Science 18, 168–173.CrossRefGoogle Scholar
Mir, NA, Rafiq, A, Kumar, F, Singh, V and Shukla, V (2017) Determinants of broiler chicken meat quality and factors affecting them: a review. Journal of Food Science and Technology 54, 2997–3009.CrossRefGoogle ScholarPubMed
National Research Council (1994) Nutrient Requirements of Poultry, 9th revised Edn. Washington, DC, USA: National Academy Press.Google Scholar
Nery, J, Gasco, L, Dabbou, S and Schiavone, A (2018) Protein composition and digestibility of black soldier fly larvae in broiler chickens revisited according to the recent nitrogen-protein conversion ratio. Journal of Insects as Food and Feed 4, 171–177.CrossRefGoogle Scholar
Paul, A, Frederich, M, Caparros Megido, R, Alabi, T, Malik, P, Uyttenbroeck, R, Francis, F, Blecker, C, Haubruge, E, Lognay, G and Danthine, S (2017) Insect fatty acids: a comparison of lipids from three Orthopterans and Tenebrio molitor L. larvae. Journal of Asia-Pacific Entomology 20, 337–340.CrossRefGoogle Scholar
Piccolo, G, Iaconisi, V, Marono, S, Gasco, L, Loponte, R, Nizza, S, Bovera, F and Parisi, G (2017) Effect of Tenebrio molitor larvae meal on growth performance, in vivo nutrients digestibility, somatic and marketable indexes of gilthead sea bream (Sparus aurata). Animal Feed Science and Technology 226, 12–20.CrossRefGoogle Scholar
Pieterse, E, Pretorius, Q, Hoffman, LC and Drew, DW (2014) The carcass quality, meat quality and sensory characteristics of broilers raised on diets containing either Musca domestica larvae meal, fish meal or soya bean meal as the main protein source. Animal Production Science 54, 622–628.CrossRefGoogle Scholar
Renna, M, Cornale, P, Lussiana, C, Malfatto, V, Fortina, R, Mimosi, A and Battaglini, LM (2012) Use of Pisum sativum (L.) as alternative protein resource in diets for dairy sheep: effects on milk yield, gross composition and fatty acid profile. Small Ruminant Research 102, 142–150.CrossRefGoogle Scholar
Renna, M, Gasmi-Boubaker, A, Lussiana, C, Battaglini, LM, Belfayez, K and Fortina, R (2014) Fatty acid composition of the seed oils of selected Vicia L. taxa from Tunisia. Italian Journal of Animal Science 13, 308–316.CrossRefGoogle Scholar
Renna, M, Brugiapaglia, A, Zanardi, E, Destefanis, G, Prandini, A, Moschini, M, Sigolo, S and Lussiana, C (2019) Fatty acid profile, meat quality and flavour acceptability of beef from double-muscled Piemontese young bulls fed ground flaxseed. Italian Journal of Animal Science 18, 355–365.CrossRefGoogle Scholar
Schiavone, A, Chiarini, R, Marzoni, M, Castillo, A., Tassone, S. and Romboli, I (2007) Breast meat traits of Muscovy ducks fed on a microalga (Crypthecodinium cohnii) meal supplemented diet. British Poultry Science 48, 573–579.CrossRefGoogle ScholarPubMed
Schiavone, A, Marzoni, M, Castillo, A, Nery, J and Romboli, I (2010) Dietary lipid sources and vitamin E affect fatty acid composition or lipid stability of breast meat from Muscovy duck. Canadian Journal of Animal Science 90, 371–378.CrossRefGoogle Scholar
Schiavone, A, De Marco, M, Martínez, S, Dabbou, S, Renna, M, Madrid, J, Hernandez, F, Rotolo, L, Costa, P, Gai, F and Gasco, L (2017a) Nutritional value of a partially defatted and a highly defatted black soldier fly larvae (Hermetia illucens L.) meal for broiler chickens: apparent nutrient digestibility, apparent metabolizable energy and apparent ileal amino acid digestibility. Journal of Animal Science and Biotechnology 8, 897–905.CrossRefGoogle Scholar
Schiavone, A, Cullere, M, De Marco, M, Meneguz, M, Biasato, I, Bergagna, S, Dezzutto, D, Gai, F, Dabbou, S, Gasco, L and Dalle Zotte, A (2017b) Partial or total replacement of soybean oil by black soldier fly larvae (Hermetia illucens L.) fat in broiler diets: effect on growth performances, feed-choice, blood traits, carcass characteristics and meat quality. Italian Journal of Animal Science 16, 93–100.CrossRefGoogle Scholar
Schiavone, A, Dabbou, S, De Marco, M, Cullere, M, Biasato, I, Biasibetti, E, Capucchio, MT, Bergagna, S, Dezzutto, D, Meneguz, M, Gai, F, Dalle Zotte, A and Gasco, L (2018) Black soldier fly (Hermetia illucens L.) larva fat inclusion in finisher broiler chicken diet as an alternative fat source. Animal: An International Journal of Animal Bioscience 12, 2032–2039.CrossRefGoogle ScholarPubMed
Sossidou, EN, Dal Bosco, A, Elson, HA and Fontes, CMGA (2011) Pasture-based systems for poultry production: implications and perspectives. World's Poultry Science Journal 67, 47–57.CrossRefGoogle Scholar
Turley, J and Thompson, J (2015) Nutrition: Your Life Science, 2nd Edn. Boston. USA: Cengage Learning, pp. 97–168.Google Scholar
Ulbricht, TL and Southgate, DAT (1991) Coronary heart disease: seven dietary factors. Lancet 338, 985–992.CrossRefGoogle ScholarPubMed
van Huis, A and Oonincx, DGAB (2017) The environmental sustainability of insects as food and feed. A review. Agronomy for Sustainable Development 37, 1–14.CrossRefGoogle Scholar
Verbeke, W, Spranghers, T, De Clercq, P, De Smet, S, Sas, B and Eeckhout, M (2015) Insects in animal feed: acceptance and its determinants among farmers, agriculture sector stakeholders and citizens. Animal Feed Science and Technology 204, 72–87.CrossRefGoogle Scholar