PhD in Veterinary Sciences for Animal Health and Food Safety

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Supervisor

Curriculum vitae

Phd thesis

The global poultry industry faces significant challenges related to environmental, economic, and social sustainability. The rising demand for animal protein necessitates a reevaluation of husbandry practices and feeding strategies to mitigate the environmental impact of poultry production. This research, conducted within the SUSTAvianFEED project, explores sustainable protein alternatives for Mediterranean native poultry breeds, focusing on the use of black soldier fly larvae (BSFL) as an innovative protein source. The project aims to develop advanced feeding strategies that reduce dependency on soybean meal by incorporating more sustainable and locally available ingredients. This study assesses both the nutritional and economic implications of these alternatives while analyzing their effects on animal physiology, behavior, and metabolism. By thoroughly examining their nutritional properties and comparing them to conventional protein sources, this research provides a comprehensive evaluation of their effectiveness in poultry feeding. Additionally, it explores the feasibility of implementing these feeding strategies on an industrial scale and their potential impact on the global animal protein market.

The primary objective was to evaluate the impact of partially or completely replacing soybean meal with alternative protein sources on growth performance, intestinal health, meat quality, and overall animal welfare. To achieve this, four dietary regimens were tested on 192 specimens of Bianca di Saluzzo, a slow-growing Italian native breed. The first group was a control group fed a standard commercial diet. The second group received a soy-free diet based on alternative plant proteins. The third group was fed the same soy-free diet supplemented with dehydrated BSFL, while the fourth group received a soy-free diet enriched with live BSFL. The effects of these diets were evaluated based on production performance, meat quality, and physiological parameters. In addition, metabolic aspects related to protein source consumption were assessed by analyzing the lipid and protein profiles of blood samples and examining intestinal microbiota modulation, with a notable increase in Faecalibacterium observed in chickens fed with live larvae​. Further biochemical analyses highlighted variations in digestive efficiency and nutrient assimilation. The potential role of chitin content in larvae as a modulating factor for intestinal health and protein absorption was also explored.

The results demonstrated that replacing soybean meal with alternative proteins did not compromise growth performance. Furthermore, BSFL supplementation significantly improved intestinal health, contributing to a better-balanced microbiota and an increased production of beneficial volatile fatty acids. Meat quality was comparable or even superior to that obtained with conventional diets, with enhanced lipid profiles and improved sensory attributes. Notably, chickens fed live larvae exhibited more natural behaviors, such as increased foraging and exploration, leading to better welfare outcomes. Behavioral assessments revealed greater vitality and reduced stress levels among these birds compared to the control group​. Moreover, the study highlighted a stronger preference for live larvae over dehydrated ones, suggesting important implications for farm feed management. Additional research assessed the presentation of larvae to optimize feed efficiency and maximize growth potential. From an environmental perspective, a Life Cycle Assessment (LCA) was conducted to evaluate the ecological footprint of the alternative diets compared to the conventional soybean-based diet. Results showed that eliminating soy significantly reduced environmental impact, making poultry farming more sustainable​. The use of insects as a protein source presents an opportunity to establish a closed-loop system in the agri-food sector, reducing overall supply chain emissions. The study further demonstrated that incorporating insect larvae in poultry diets reduces reliance on intensive soybean cultivation, thus helping to combat deforestation and decreasing pesticide usage, leading to enhanced biodiversity and improved soil quality​. Further investigations into livestock environmental management indicate that larvae-based feeds could be integrated into circular economy models, enhancing the overall sustainability of the poultry industry. Future studies should assess the scalability of this approach across other native poultry breeds and its long-term economic viability in various production systems. This study underscores the potential of soy-free diets enriched with locally sourced plant proteins as a viable alternative for poultry nutrition. The findings confirm that chickens can adapt effectively to these new formulations without any adverse effects on growth performance or meat quality. At the same time, BSFL supplementation offers additional benefits, particularly in improving intestinal health and animal welfare, making it a highly promising alternative protein source. The large-scale adoption of these strategies could revolutionize the poultry industry, reducing environmental impacts while strengthening local production systems. Additionally, enhanced consumer education and awareness could facilitate the acceptance of insect-fed and soy-free poultry products, unlocking new market opportunities for a more sustainable and efficient poultry sector.

Research activities

Publications that constitute the experimental chapters of the thesis:

1. Improving sustainability in autochthonous slow-growing chicken farming: Exploring new frontiers through the use of alternative dietary proteins. Fiorilla E, Gariglio M, Martinez-Miro S, Rosique C, Madrid J, Montalban A, Biasato I, Bongiorno V, Cappone EE, Soglia D, Schiavone A (2024). Journal of Cleaner Production. 434:140041. https://doi.org/10.1016/j.jclepro.2023.140041 First Author - Q1 - IF: 9.7 (2023)
2. Dehydrated and live black soldier fly larvae as environmental enrichment in indigenous slow-growing chickens: performance, gut health, and chitinolytic enzyme activity. Fiorilla E, Gariglio M, Gai F, Zambotto V, Bongiorno V, Cappone EE, Biasato I, Bergagna S, Madrid J, Martinez-Miró S, Capucchio MT, Ippolito D, Fabrikov D, Castillo LL, Cortes J, Coudron C, Schiavone A (2024). 18 (8): 101239. https://doi.org/10.1016/j.animal.2024.101239 First Author - Q1 - IF: 4 (2023)
3. Breaking down barriers: live or dehydrated dietary whole black soldier fly larvae supplementation in slow growing chickens preserve meat quality and sensory traits. Fiorilla E, Gariglio M, Gai F, Zambotto V, Bongiorno V, Cappone EE, Rødbotten R, Koga S, Rieder A, Tengstrand E, Pozzo S, Daniele GM, Cianciabella M, Predieri S, Forte C, Schiavone A (2024). Poultry Science. https://doi.org/10.1016/j.psj.2024.104120 First Author - Q1 - IF: 3.8 (2023)
4. Unraveling the Chicken Meat Volatilome with Nanostructured Sensors: Impact of Live and Dehydrated Insect Larvae Feeding. Genzardi D, Núñez Carmona E, Poeta E, Gai F, Caruso I, Fiorilla E, Schiavone A, Sberveglieri V (2024). Sensors. 24 (15). https://doi.org/10.3390/s24154921 Co-Author - Q1 - IF: 3.4 (2023)
5. Beyond soybean meal: investigating the effects of dietary protein alternatives on gut health, liver function and microbiota in traditional slow-growing chicken breeds. Fiorilla, E., Ferrocino, M. Gariglio, F. Gai, V. Zambotto, L. Ozella, I. Franciosa, M. Giribaldi, S. Antoniazzi, F. Raspa, E. E. Cappone, D. Fabrikov, V. Bongiorno, D. Ippolito, C. Sferra, M. T. Capucchio, and A. Schiavone. (2024).  Italian Journal of Animal Science 23:1635–1648 https://doi.org/10.1080/1828051X.2024.2416582. First Author - Q1 - IF: 2.3 (2023)
6. Black soldier fly larvae: a one health approach to investigate gut, and organ health and meat quality response in slow-growing chickens. Fiorilla, E., Ferrocino, M. Gariglio, F. Gai, V. Zambotto, L. Ozella, I. Franciosa, M. Giribaldi, S. Antoniazzi, F. Raspa, E. E. Cappone, D. Fabrikov, S. Pozzo, V. Bongiorno, A. Calissano, D. Ippolito, S. Bergagna, K. Srikanthithasan, C. Forte, M. T. Capucchio, and A. Schiavone (2024). BMC Veterinary Research 20:580 https://doi.org/10.1186/s12917-024-04394-0. First Author - Q1 - IF: 2.6 (2023)
7. New horizons in live and dehydrated black soldier fly larvae usage: behavioral and welfare implications in “Bianca di Saluzzo” cockerels. Bongiorno, , Fiorilla^, E., Gariglio^, M., Zambotto^, V., Cappone, E.E., Bergagna, S., Manenti, I., Macchi, E., Gai, F., Schiavone, A. (2025). Plos One. 10.1371/journal.pone.0318793 Corresponding Author - Q1 - IF: 2.9

Other publications on ISI journals achieved during the PhD program:

1. Dietary processed former foodstuffs for broilers: impacts on growth performance, digestibility, hematobiochemical profiles and liver gene abundance. Srikanthithasan K, Gariglio M, Diaz Vicuna E, Fiorilla E, Miniscalco B, Zambotto V, Cappone EE, Stoppani N, Soglia D, Raspa F, Nery J, Giorgino A, Sala R, Martínez AL, Madrid Sanchez J, Schiavone, A (2024). Journal of Animal Science and Biotechnology 15, 122. https://doi.org/10.1186/s40104-024-01081-w Co-Author - Q1 - IF: 6.3 (2023)
2. The Influence of Alternative Diets and Whole Dry Black Soldier Fly Larvae (Hermetia illucens) on the Production Performance, Blood Status, and Egg Quality of Laying Hens. Montalbán A, Madrid J, Hernández F, Schiavone A, Ruiz E, Sánchez CJ, Ayala L, Fiorilla E, Martínez-Miró S. (2024). 14(17):2550. https://doi.org/10.3390/ani14172550 Co-Author - Q1 - IF: 2.7 (2023)
3. Effects of housing systems on behaviour and welfare of autochthonous laying hens and a commercial hybrid. Fiorilla E, Ozella L, Sirri F, Zampiga M, Piscitelli R, Tarantola M, Ponzio P, Mugnai C (2024). Applied Animal Behaviour Science. 274:106247. https://doi.org/10.1016/j.applanim.2024.106247 First Author - Q1 - IF: 2.2 (2023)
4. Behaviour and welfare assessment of autochthonous slow-growing rabbits: The role of housing systems. Ozella L, Sartore S, Macchi E, Manenti I, Mioletti S, Miniscalco B, Crosetto R, Ponzio P, Fiorilla E, Mugnai C (2024). Plos One. 19 (7): 1–17. https://doi.org/10.1371/journal.pone.0307456 Corresponding Author - Q1 - IF: 2.9
5. Former foodstuffs in feed: a minireview of recent findings. Srikanthithasan K, Giorgino A, Fiorilla E, Ozella L, Gariglio M, Schiavone A, Marín ALM, Diaz Vicuna E, Forte C (2024). Environmental Science and Pollution Research. 31(16):23322–33. https://doi.org/10.1007/s11356-024-32695-2 Co-Author - Q1 - IF: 5.8 (2022)
6. Effect of rearing systems on immune status, stress parameters, intestinal morphology, and mortality in conventional and local chicken breeds. Stefanetti V, Cartoni Mancinelli A, Pascucci L, Menchetti L, Castellini C, Mugnai C, Fiorilla E, Miniscalco B, Chiattelli D, Franciosini MP, Proietti PC (2023). Poultry Science. 102 (12): 103110. https://doi.org/10.1016/j.psj.2023.103110 Co-Author - Q1 - IF: 3.8 (2023)
7. Productive Performances of Slow-Growing Chicken Breeds and Their Crosses with a Commercial Strain in Conventional and Free-Range Farming Systems. Fiorilla E, Birolo M, Ala U, Xiccato G, Trocino A, Schiavone A, Mugnai C (2023). 13 (15). https://doi.org/10.3390/ani13152540 First Author - Q1 - IF: 2.7 (2023)
8. Effect of feeding a thermomechanical, enzyme-facilitated, co-processed yeast and soybean meal on growth performance, organ weights, leg health and gut development of broiler chickens. Colombino E, Karimi M, Ton Nu MA, Tilatti A, Bellezza Oddon S, Calini F, Bergamino C, Fiorilla E, Gariglio M, Gai F, Capucchio MT, Schiavone A, Gasco L, Biasato I (2023). Poultry Science 102, 102578. https://doi.org/10.1016/j.psj.2023.102578 Co-Author - Q1 - IF: 3.8 (2023)
9. Welfare implications for broiler chickens reared in an insect larvae-enriched environment: Focus on bird behaviour, plumage status, leg health, and excreta corticosterone. Biasato I, Bellezza Oddon S, Chemello G, Gariglio M, Fiorilla E, Dabbou S, Pipan M, Dekleva D, Macchi E, Gasco L, Schiavone A (2022). Frontiers in Physiology. https://doi.org/10.3389/fphys.2022.930158 Co-Author - Q1 - IF: 3.2 (2023)
10. Poultry biodiversity for alternative farming systems development. Fiorilla E, Cartoni Mancinelli A, Birolo M, Castellini C, Soglia D, Macchi E, Mioletti S, Miniscalco B, Sartore S, Franco R, Nurisso S, Baruchello M, Tarantola M, Sacchi P, Schiavone A, Mugnai C. (2022). E3S Web of Conferences. 335:00004. https://doi.org/10.1051/e3sconf/202233500004 First Author – Q3 - IF: 0.9 (2023)
11. Black soldier fly and yellow mealworm live larvae for broiler chickens: Effects on bird performance and health status. Bellezza Oddon S, Biasato I, Imarisio A, Pipan M, Dekleva D, Colombino E, Capucchio MT, Meneguz M, Bergagna S, Barbero R, Gariglio M, Dabbou S, Fiorilla E, Gasco L, Schiavone A (2021). Journal of Animal Physiology and Animal Nutrition. 105 (S1): 10–18. https://doi.org/10.1111/jpn.13567 Co-Author - Q1 - IF: 2.2 (2023)

Publications