Effect of energy enrichment of dairy cattle manure on the productive performance and nutritional characterization of Musca domestica larval mealAbstract
Insect larva production for animal feed represents a sustainable alternative to the growing demand for protein. This research evaluated the productive performance of housefly (Musca domestica) larvae reared on dairy cattle manure (DCM) under different levels of energy enrichment, alongside a nutritional characterization of the basal meal. A completely randomized design was employed with four treatments for productive variables: pure DCM (T0), DCM + 5% oil (T1), DCM + 5% molasses (T2), and DCM + 5% oil + 5% molasses (T3). Following bioconversion, the pure substrate (T0) exhibited a marginal reduction of 8% in both crude protein and crude fat, while nitrogen-free extract decreased by 22%. Individual weight and biomass production increased significantly (P < 0.01) with energy enrichment; T3 stood out with a larval weight of 17.19 mg and a productivity of 9.15 g/kg of substrate, representing increases of 123% and 244% compared to the control, respectively. A descriptive nutritional characterization was performed on the housefly larval meal (HFLM) produced from the basal substrate (T0), which presented 55.7% crude protein and 28.30 g/100g total fat. The amino acid profile was competitive against conventional sources, highlighting high levels of arginine (6.99 g/100g) and lysine (3.55 g/100g). The lipid profile was predominantly polyunsaturated, with an omega-6:omega-3 ratio of 1.4:1. Regarding minerals, HFLM proved to be rich in phosphorus (0.93 g/100g) but limited in calcium (0.14 g/100g). Microbiological analysis showed the absence of Salmonella spp., although levels of coliforms (1.1 x 103 CFU/g) and Clostridium perfringens (250 CFU/g) exceeded sanitary limits. It is concluded that manure enrichment improves larval productive indicators; however, the resulting meal requires strict sanitization protocols to guarantee its safety, and its potential as a protein source is supported by the competitive nutritional profile of the basal HFLM.
Keywords:
bioconversion; amino acids; molasses; organic waste; food safety; polyunsaturated fat; phosphorus
Resumo
A produção de larvas de insetos para alimentação animal representa uma alternativa sustentável à crescente demanda por proteína. Esta pesquisa avaliou o desempenho produtivo de larvas de mosca-doméstica (Musca domestica) criadas em esterco de bovinos leiteiros (EBL) sob diferentes níveis de enriquecimento energético, juntamente com a caracterização nutricional da farinha basal. Foi empregado um delineamento inteiramente casualizado com quatro tratamentos para as variáveis produtivas: EBL puro (T0), EBL + 5% de óleo (T1), EBL + 5% de melaço (T2) e EBL + 5% de óleo + 5% de melaço (T3). Após a bioconversão, o substrato puro (T0) apresentou uma redução marginal de 8% tanto na proteína bruta quanto na gordura bruta, enquanto o extrato livre de nitrogênio diminuiu 22%. O peso individual e a produção de biomassa aumentaram significativamente (P < 0,01) com o enriquecimento energético. O tratamento T3 destacou-se com um peso larval de 17,19 mg e uma produtividade de 9,15 g/kg de substrato, representando aumentos de 123% e 244% em comparação com o controle, respectivamente. Uma caracterização nutricional descritiva foi realizada na farinha de larvas de mosca-doméstica (FLMD) produzida a partir do substrato basal (T0), que apresentou 55,7% de proteína bruta e 28,30 g/100 g de gordura total. O perfil de aminoácidos mostrou-se competitivo em relação às fontes convencionais, destacando-se os altos níveis de arginina (6,99 g/100 g) e lisina (3,55 g/100 g). O perfil lipídico foi predominantemente poli-insaturado, com razão ômega-6:ômega-3 de 1,4:1. Em relação aos minerais, a FLMD mostrou-se rica em fósforo (0,93 g/100 g), mas limitada em cálcio (0,14 g/100 g). A análise microbiológica evidenciou ausência de Salmonella spp., embora os níveis de coliformes (1,1 x 103 UFC/g) e Clostridium perfringens (250 UFC/g) tenham ultrapassado os limites sanitários. Conclui-se que o enriquecimento com esterco melhora os indicadores produtivos larvais; no entanto, a farinha resultante requer protocolos rigorosos de higienização para garantir a sua segurança, e o seu potencial como fonte de proteína é respaldado pelo perfil nutricional competitivo da HFLM basal.
Palavras-chave:
bioconversão; aminoácidos; melaço; resíduos orgânicos; segurança alimentar; gordura poli-insaturada; fósforo
1. Introduction
In the current scenario of population growth and sustained demand for sustainable protein sources, animal production faces the challenge of ensuring food security by optimizing the use of natural resources (Gil et al., 2024). In this context, zootechnical entomology has emerged as a strategic alternative, highlighting the use of saprophagous insects such as the housefly (Musca domestica) due to their efficiency in the bioconversion of organic waste into nutrient-rich biomass (Zafeiriadis and Athanassiou, 2025). The production of housefly larval meal (HFLM) from agricultural waste, such as dairy cattle manure, represents an opportunity to valorize by-products abundant in organic matter.
Various studies have demonstrated that M. domestica larvae transform livestock waste into biomass with a nutritional value competitive with conventional sources such as fishmeal and soybean meal (Hussein et al., 2017). The crude protein content in HFLM can reach 60%, with a favorable amino acid profile characterized by a high lysine concentration and an adequate methionine balance (Pieterse and Pretorius, 2014), which are critical elements for diet formulation in monogastrics. In this regard, Hall et al. (2018) reported high standardized ileal digestibility of these amino acids in broilers, without adverse effects on productive performance.
The quality of the rearing substrate directly determines the larval nutritional profile. Dairy cattle manure is a balanced medium that provides essential nitrogen and phosphorus for larval growth (Noumbissi et al., 2021). Furthermore, bioconversion reduces the organic load of waste, mitigating environmental impact (van Zanten et al., 2015). Previous studies have explored substrate supplementation to improve yield; for instance, the use of bovine blood has achieved crude protein levels exceeding 45-53% and fats of 18% (Alamba et al., 2024; Ali et al., 2024). Likewise, the inclusion of HFLM in animal diets has shown favorable sensory acceptance in finished products, such as poultry meat (Radulović et al., 2018).
While dairy cattle manure is a viable substrate, its high fiber content and variable nutrient density often act as a limiting factor for optimal larval growth. Previous research indicates that supplementing insect substrates with readily fermentable carbohydrates and lipids can significantly enhance biomass accumulation and nutrient deposition (Hussein et al., 2017). In this study, we hypothesize that the strategic enrichment of manure with molasses (as a soluble carbon source) and vegetable oil (as a concentrated energy source) will alleviate the inherent energy limitations of pure manure, optimizing the energy-to-protein ratio and the resulting productive performance. Consequently, this study evaluated the effect of enrichment on M. domestica performance, while providing a comprehensive descriptive characterization of the basal larval meal (T0) to establish a reference baseline.
2. Materials and Methods
2.1. Study site and environmental conditions
The research was conducted at the Dairy Cattle Experimental Workshop of the Universidad Nacional José Faustino Sánchez Carrión (Huacho, Peru; -11.124391, -77.606939, 50 m a.s.l.). The study took place between July and September 2023, characterized by temperatures ranging from 16.2 °C to 27.6 °C (average 23.4 °C) and a relative humidity between 78.4% and 94.6% (average 87.2%). Climatological data were obtained from the SENAMHI meteorological station located at the Universidad Nacional José Faustino Sánchez Carrión (UNJFSC), Huacho.
2.2. Experimental design
The study was divided into two consecutive stages: (1) evaluation of the productive efficiency of Musca domestica larvae on enriched substrates, and (2) nutritional characterization and safety assessment of the larval meal obtained from the control treatment.
For the first stage, a completely randomized design was used with four treatments and five replicates each (n=20 experimental units). The experimental unit consisted of a black polyethylene bag containing 1 kg of processed substrate. The evaluated treatments were: T0: Dairy cattle manure (control); T1: Manure + 5% residual vegetable oil; T2: Manure + 5% molasses; and T3: Manure + 5% residual oil + 5% molasses.
2.3. Substrate preparation and larval collection
Fresh manure was collected and arranged outdoors in 10-kg piles. Additives were incorporated according to the treatment and homogenized manually. After 24 h of exposure to allow for natural oviposition, the piles were covered with plastic sheets to stabilize moisture and temperature. On the fifth day, 1 kg was extracted from each pile (replicate) and transferred to polyethylene bags with 3-mm basal perforations. The bags were suspended from overhead supports, allowing L3 stage larvae to fall by negative geotaxis into collection trays for three consecutive days.
2.4. Processing and larval meal production
Collected larvae were washed with potable water using fine-mesh sieves to remove debris and substrate residues. After a 4-h draining period in the shade, the larvae were distributed in stainless steel trays and subjected to dehydration in a forced-air drying oven (H – Hornos y Servicios, 481 kg capacity) at a constant temperature of 60 °C for 52 h. Once the desired residual moisture was reached, the dried larvae were processed in a manual blade mill to obtain a fine-textured meal (particle size < 1 mm), which was stored in airtight containers for subsequent analysis.
2.5. Chemical and microbiological analysis
2.5.1. Proximate composition and energy calculation
Proximate bromatological analysis followed AOAC (2005) protocols. Gross energy (GE) was calculated using the AEC (1978) equation (Equation 1):
where: CP = Crude Protein; EE = Ether Extract; CF = Crude Fiber; NFE = Nitrogen-Free Extract.
For enriched substrates, reference caloric values from Rostagno et al. (2017) were used. This proximate analysis was performed on the larval meal from all experimental treatments (T0, T1, T2, and T3). Additionally, the characterization of the dairy cattle manure (both before and after the bioconversion process) was conducted for the control treatment (T0) to evaluate the substrate's nutritional flux.
2.5.2. Specialized nutritional characterization of basal HFLM
To establish a baseline for the non-enriched substrate model, specialized analyses were performed exclusively on the housefly larval meal (HFLM) derived from the control treatment (T0). The amino acid profile was determined by the AOAC 984.13 method using an ion-exchange amino acid analyzer. The fatty acid profile was analyzed via gas chromatography with flame ionization detection (GC-FID, Model 7890B, Agilent Technologies, USA) following the AOAC 996.06 method. This specific protocol includes an initial acid hydrolysis, ensuring the release of structural lipids from the chitin-protein matrix. Furthermore, macrominerals (Ca, P, Na) were determined by atomic absorption spectrophotometry (AOAC 975.03/985.35).
2.5.3. Microbiological safety evaluation
The microbiological quality of the basal HFLM was evaluated to determine its safety as a feed ingredient. The analysis of Salmonella spp., coliforms, and Clostridium perfringens was performed according to ICMSF (1978, 1983) standards. This evaluation was conducted on the meal derived from the control treatment under the described experimental conditions.
2.5.4. Sampling and statistical approach
All nutritional determinations were carried out using pooled samples per treatment, analyzed in technical duplicate (n=2). Due to this sampling methodology, the chemical composition results—specifically amino acids, fatty acids, minerals, and safety—are presented descriptively as mean values. This approach provides a rigorous baseline characterization for the evaluated groups, while inferential statistics were reserved for the productive performance section.
2.6. Statistical analysis
Data were analyzed using a stepwise approach. For production variables (individual weight and total biomass), the assumptions of normality (Shapiro-Wilk test) and homogeneity of variances (Levene's test) were verified. Since both assumptions were met, a one-way Analysis of Variance (ANOVA) was applied. In case of significant differences, Tukey's multiple comparison test (P < 0.05) was used. The nutritional characterization of the meal was analyzed using descriptive statistics (mean and standard deviation). All procedures were executed in jamovi statistical software (The Jamovi Project, 2022).
3. Results
3.1. Substrate bioconversion (control treatment)
Following bioconversion with M. domestica, the dairy cattle manure (T0) exhibited a marginal reduction of 8% in both crude protein (from 16.46% to 15.07%) and crude fat (from 0.87% to 0.80%). Nitrogen-free extract (NFE) was the fraction with the highest utilization rate, decreasing by 22% (from 50.76% to 39.50%), which suggests a preferential consumption of easily hydrolyzed carbohydrates for larval metabolism and growth. Conversely, crude fiber showed a relative concentration increase of 168% (from 8.25% to 22.09%). This change does not imply absolute fiber synthesis, but rather a concentration effect of structural carbohydrates that were not effectively degraded during the bioconversion process, while other organic components were significantly depleted (Table 1).
Proximate chemical composition (dry matter basis) of dairy cow manure before and after Musca domestica larval bioconversion in the control group.
3.2. Productive performance across treatments
Dairy cattle manure enrichment with energy sources (oil and molasses) significantly increased housefly larval production. As detailed in Table 2, both individual larval weight and total production per kilogram of substrate in the treatment enriched with the combination of oil and molasses (T3) were superior to those recorded in the control group (T0) and the treatments with only oil (T1) or only molasses (T2). Specifically, the T3 treatment reached a larval weight of 17.19 ± 0.5 mg and a productivity of 9.15 ± 0.8 g/kg, representing increases of 123% and 244% compared to the control, respectively. Furthermore, the weight of larvae produced with the addition of oil (T1: 13.47 ± 0.4 mg) was significantly higher compared to the manure-only treatment (T0: 7.69 ± 0.7 mg) or the molasses-enriched treatment (T2: 11.44 ± 0.4 mg) (P < 0.01; Table 2).
Effect of dairy cattle manure enrichment on housefly (Musca domestica) larval production (n = 5).
3.3. Proximate composition of HFLM by treatment
The proximate analysis of the housefly larval meal across treatments is presented in Table 3. Substrate enrichment resulted in numerical variations in the nutritional profile, particularly regarding fat and energy content. Crude fat values ranged from 13.30% in the control group (T0) to 21.47% in larvae reared on molasses (T2) and 18.86% with oil (T1). In contrast, crude protein and ash levels tended to be lower in the enriched treatments compared to the control (T0: 55.81% protein and 6.63% ash), with minimum values of 51.12% for protein and 5.93% for ash recorded in T2. The gross energy values showed a numerical increase with enrichment, reaching 5,278 kcal/kg in the molasses treatment (T2) compared to 4,896 kcal/kg in the basal HFLM. Variations in crude fiber and NFE were relative to the fluctuations in fat content, with T3 showing an NFE increase of up to 148% compared to the control.
Chemical composition and energy value of housefly (Musca domestica) larval meal according to the substrate used (As-fed basis).
3.4. Amino acid and fatty acid profiles of basal HFLM
The amino acid profile of the HFLM (T0) was compared descriptively with conventional protein sources (Table 4). The meal presented a profile comparable to fishmeal, displaying numerically higher contents of lysine, tryptophan, and isoleucine, and notably higher concentrations of arginine and the sum of phenylalanine and tyrosine. When contrasted with soybean meal, the larval meal showed higher concentrations of most essential amino acids, with the exception of tryptophan.
Amino acid profile (g/100g dry matter) of HFLM obtained from the control group compared to conventional sources.
Regarding the lipid fraction of the HFLM derived from the control group (Table 5), a predominance of unsaturated fatty acids was observed. Polyunsaturated fatty acids (PUFAs) were the main components, with linoleic and linolenic acids being the most prominent. Conversely, monounsaturated fatty acids (MUFAs) were found at lower levels, while components such as myristic, palmitic, and oleic acids were below the analytical limit of detection. The meal was characterized by a total omega-6 content of 12.43 g/100 g and omega-3 of 8.42 g/100 g, resulting in an omega-6:omega-3 ratio of 1.4:1.
It is essential to clarify the discrepancy between the ether extract content in Table 3 (13.30%) and the total lipids reported in Table 5 (28.30 g/100 g). This variation is methodological in nature; while the proximate analysis quantifies free fats on a wet basis, the AOAC 996.06 method employs acid hydrolysis prior to gas chromatography on a dry basis. This procedure facilitates the release of structural fatty acids bound to the chitin and protein matrix of the larva, resulting in a more exhaustive lipid recovery (Li et al., 2019).
3.5. Mineral content of basal HFLM
The macromineral characterization of the housefly larval meal (T0) identified phosphorus as the most abundant element (Table 6). This was followed in quantitative importance by sodium and calcium, with the latter presenting the lowest concentration among the evaluated minerals. These values characterize the meal as a mineral source rich in phosphorus but with limited calcium supply.
3.6. Microbiological safety of basal HFLM
Microbiological analysis of the HFLM produced from the basal substrate showed the absence of Salmonella spp. (Table 7). The total coliform count was 1.1 x 103 CFU/g, while the Clostridium perfringens concentration was 2.5 x 102 CFU/g. These values describe the microbial load of the larvae reared under the specific experimental conditions of this study.
4. Discussion
4.1. Substrate bioconversion (control treatment)
The chemical composition of manure, contingent upon the host's diet and gastrointestinal physiology, determines the biomass potential of M. domestica (Hussein et al., 2017). In this study, dairy cattle manure proved to be a viable medium, although the persistence of a substantial protein fraction (15.07%) and a marginal reduction of only 8% suggest a partial utilization of nitrogenous nutrients. This phenomenon could be related to a nutrient imbalance, possibly due to a lower availability of easily accessible carbon sources relative to the nitrogen content, as the efficiency of nutrient recovery in Diptera is highly dependent on the initial substrate's complexity (Yan et al., 2026). In support of this, NFE showed the highest utilization rate (-22%), which may indicate a preferential consumption of easily hydrolyzed carbohydrates for larval energy demands. Consequently, the 168% increase in residual crude fiber suggests that structural carbohydrates were not effectively degraded, which might have limited the overall bioconversion of the available protein (Table 1).
4.2. Productive performance across treatments
Similarly to higher vertebrates, insects require a balance of nutrients to optimize their development (Hussein et al., 2017). In the present study, substrate supplementation with exogenous energy sources (oil and molasses) significantly enhanced larval productive performance. This increase suggests that the availability of readily fermentable carbohydrates and energy-dense lipids may fulfill basal metabolic demands, potentially channeling more resources toward biomass accumulation. Strategic enrichment appears to compensate for the inherent energy density limitations of pure manure, resulting in higher nutrient utilization efficiency and final larval weight.
4.3. Proximate composition of HFLM by treatment
Crude fat was the nutritional parameter most influenced by manure enrichment. Supplementation with molasses and oil increased lipid levels, which aligns with findings by Thompson and Simpson (2009) regarding the larval capacity to accumulate fat reserves when substrates are energy-rich. Unlike conventional protein sources, this meal is characterized by its crude fiber content, primarily composed of chitin. This nitrogenous structural biopolymer is associated with the acid detergent fiber fraction in insects (Finke, 2007). Finally, the observed average composition (60.3% protein and 20.0% fat on a dry matter basis) aligns with findings by Hussein et al. (2017), confirming the nutritional stability of this feedstock under the evaluated model.
4.4. Amino acid and fatty acid profiles of basal HFLM
The amino acid profile of HFLM proved to be competitive against conventional protein sources in terms of gross chemical concentration. According to the reference values reported by Rostagno et al. (2017), the larval meal exhibits a composition analogous to that of fishmeal, with numerically higher contents of lysine, tryptophan, and isoleucine. Furthermore, when contrasted with soybean meal, HFLM shows higher analytical concentrations in most essential amino acids, except for tryptophan. However, it is essential to emphasize that these findings are limited to chemical composition; digestibility and bioavailability trials would be required to evaluate the actual metabolic utilization of these nutrients in specific animal diets.
Regarding the lipid fraction, the baseline HFLM (T0) presents a profile notable for its concentration of unsaturated fats, primarily linoleic and linolenic acids. The absence of detectable levels of palmitic, oleic, and stearic acids in this specific characterization is an atypical finding, likely due to concentrations being below the analytical limit of detection. It is possible that under the specific nutritional conditions of non-enriched manure, there is a prioritized retention of polyunsaturated fractions, although this remains a hypothesis as metabolic pathways were not directly measured. The observed omega-6 to omega-3 ratio of 1.4:1 is analogous to that reported for standard fishmeal (Rostagno et al., 2017), highlighting its interesting chemical profile.
The discrepancy between lipid levels obtained through gravimetric (13.30%) and chromatographic (28.30%) methods (AOAC 996.06) is a documented phenomenon stemming from the biological matrix complexity of insects. The M. domestica larva possesses a chitin-protein exoskeleton where a significant fraction of lipids may be integrated into lipoprotein complexes (Li et al., 2019; Hall et al., 2018). While the Soxhlet method (Table 3) primarily solubilizes free fats, the acid hydrolysis in the AOAC method is critical for releasing chemically bound fatty acids (Hall et al., 2018; Fitches et al., 2019). From an analytical perspective, the chromatographic values reflect a more exhaustive recovery of the fatty acids present in the meal.
4.5. Mineral content of basal HFLM
The macromineral profile of HFLM observed in this study characterizes this material as a phosphorus-rich but calcium-deficient source, which is consistent with reports by Ahmad et al. (2022). When benchmarked against the nutritional standards of Rostagno et al. (2017), HFLM provides approximately 3% of the calcium and 39% of the phosphorus levels typically found in standard fishmeal. This analytical mineral disparity is a factor that must be addressed through strategic supplementation during feed formulation to ensure optimal animal performance.
4.6. Microbiological safety of basal HFLM
Houseflies are recognized as potential biological vectors of pathogens due to their contact with decaying organic matter (Monyama et al., 2023). In the present study, while Salmonella spp. was not detected, other microbiological indicators, such as coliforms and Clostridium perfringens, exceeded the safety thresholds established by certain sanitary regulations (Peru, 2008). These findings indicate that while HFLM is a promising protein source, its safety depends on the implementation of validated sanitization protocols—such as thermal treatments—to ensure the safety of the final product and compliance with microbiological standards.
5. Conclusion
Dairy cattle manure constitutes a viable basal feedstock for Musca domestica larval production; however, its efficiency is highly dependent on nutrient density. Strategic energy enrichment with a combination of oil and molasses (T3) significantly enhances productive performance, optimizing both individual larval weight and total biomass yield per kilogram of substrate. Regarding the nutritional profile, the basal larval meal (T0) exhibits an essential amino acid and polyunsaturated fatty acid composition that provides a high-quality chemical reference compared to conventional protein sources. Nevertheless, the microbiological load observed in the raw meal, characterized by coliform and Clostridium perfringens counts exceeding sanitary limits (Peru, 2008), currently restricts its direct commercial application. The viability of this meal as an animal feed ingredient is strictly contingent upon the implementation of validated sanitization and thermal processing protocols to ensure microbiological safety.
Acknowledgements
This study was funded by the research project “Zootecnia autosostenible: aplicación de insectos en dietas para la mejora de la productividad animal, utilizando energías renovables y residuos orgánicos” from the scientific and/or technological research project contest for professors, funded with determined resources, approved by the University Council Presidency Resolution No. 010-2020-P-CU-UNJFSC.
Data Availability Statement
Data availability statement: All data generated or analyzed during this study are included in this published article.
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Editor:
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