Impact of diets incorporating Black Soldier Fly larvae meal and lactic acid bacteria-supplemented drinking water on the health profile and performance of IPB D1 chickens

Nella Khairati¹, Muhammad Ridla^2,3*, Widya Hermana² and Nahrowi^2,3

¹ Graduate School of Animal Nutrition and Feed Science, Faculty of Animal Science, IPB University, Kampus Dramaga, Bogor 16680, Indonesia
² Department of Animal Nutrition and Feed Technology, Faculty of Animal Science, IPB University, Bogor 16680, Indonesia
³ Center for Tropical Animal Studies (CENTRAS), IPB University, Jl. Raya Pajajaran, Bogor 16153, Indonesia
* hmridla@apps.ipb.ac.id

Abstract

The study aimed to assess the health profile and performance of IPB D1 chickens when fed diets containing Black Soldier Fly (BSF) larvae or maggot meal, along with lactic acid bacteria (LAB) supplemented drinking water. A total of 240 IPB D1 chickens were divided into four treatment groups, each with six replications: M0L0 (control feed without LAB), M0L1 (control feed with LAB), M1L0 (treatment feed without LAB), and M1L1 (treatment feed with LAB). Chickens were provided with feed containing 15% maggot meal, and their feed intake and body weight were monitored weekly. Blood, internal organs, and carcasses were collected on day 36 for analysis. The results revealed that there were no significant differences in feed intake, body weight gain, and feed conversion ratio (FCR) among IPB D1 chickens fed with maggot meal and LAB-supplemented drinking water. The relative weights of various internal organs, including the proventriculus, gizzard, pancreas, small intestine, and caeca, showed no variations with the inclusion of maggot meal and LAB-supplemented drinking water in the diets. Similarly, there were no discernible effects on the spleen, thymus, and bursa of Fabricius due to the treatments. Additionally, feeding maggot meals and providing LAB-supplemented drinking water did not impact the eviscerated carcass of the chickens. Blood profile parameters remained unaffected by the dietary and drinking water treatments. In conclusion, incorporating maggot meal into feed at a level of up to 15% does not adversely affect the health status and performance of IPB D1 chickens. However, the potential impact of administering probiotics in drinking water remains uncertain, as no notable effects on the health and performance of IPB D1 chickens were observed.

Keywords: blood profile, immune system, local chicken, organs

Introduction

The demand for animal protein is on the rise, propelled by increasing income, population growth, and heightened public awareness of the nutritional and health benefits associated with chicken meat (Citra 2019). According to data from the Indonesian Central Statistics Agency for the years 2011-2020 (BPS 2023), the consumption of animal protein, particularly purebred chicken meat, showed an average annual increase of 2.27% per capita among the Indonesian population.

Efficient measures are crucial for meeting chicken meat production targets, and one effective strategy involves utilizing local chickens suitable for meat production, such as the IPB D1 chicken. The establishment of the IPB D1 chicken aims to enhance the role of local chickens, characterized by advantages such as excellent meat taste, disease resistance, and the ability to utilize local feed. However, a significant challenge faced by local chickens is their slow growth rate.

To address this challenge, fast-growth genes from broiler chickens (25%) were introduced to the IPB D1 through crossbreeding with three local chicken families (25% Kampung, 25% Pelung, and 25% Sentul) (Habib et al 2020). IPB D1 chickens have successfully achieved accelerated growth, reaching a slaughter weight of 1.51 kg at 12 weeks of age, as reported by Ulupi et al (2016). This achievement surpasses the weights of 0.92 kg for local chickens and 0.81 kg for native Sentul chickens, as documented by Solikin et al (2016). Additionally, IPB D1 chickens demonstrate the ability to assimilate local feed ingredients as their primary source of nutrition, while simultaneously maintaining the health aspects of livestock. Currently, common practices involving local feed ingredients include the incorporation of maggot meal in feed and the administration of probiotics in drinking water.

Maggot meal serves as a valuable source of animal protein, functioning as a substitute for fish meal or meat bone meal. Maggot meals are rich in animal protein, boasting a protein content of 42.65% (Mawaddah 2018). Protein plays a crucial role in the well-being of livestock, particularly in supporting growth and enhancing livestock endurance. The fat content in maggot meal is notably high, reaching 27.36%, in contrast to the fat content in meat bone meal (MBM), which is reported at 5.59% (Afikasari et al 2022). Additional sources indicate specific nutrient levels in maggot meal, including a minimum of 30% crude protein, 28% crude fat, 2-3% calcium, and 0.88% phosphorus (Katayane et al 2014).

Livestock survival relies not only on proper rations but also on maintaining good health conditions. The prohibition on the use of AGP poses challenges for breeders striving to achieve optimal animal production. Therefore, it is essential to explore alternatives to AGP usage to ensure both robust livestock growth and good health. One viable alternative is the incorporation of probiotics.

Augmenting the population of beneficial microbes in the digestive system can relatively reduce the presence of pathogenic microbes that may disrupt digestion. These beneficial microbes play a dominant role in the digestive tract, aiding in the digestive process and facilitating nutrient absorption. Administering probiotics at the correct dosage can assist the digestive tract in effectively utilizing nutrients without compromising the animal's health. Essentially, the mechanism of action for probiotics involves competing with other microbes for food sources, vying for adhesion sites in the small intestine, engaging in direct antagonism, and stimulating the immune system.

Notably, no prior research has investigated the impact of maggot meal and Lactic Acid Bacteria (LAB) on the health and growth performance of IPB D1 chickens. Therefore, this research aims to elucidate the health profile and performance of IPB D1 chickens when fed with feed containing maggot meal and supplemented with lactic acid bacteria (LAB) in their drinking water.

Materials and Methods

The research involved 240 IPB D1 chickens spanning from 1 to 63 days of age. During the initial 1-14 days, the chickens were fed standard broiler rations, while from day 15 to 63, they were provided with the treatment diets. The nutritional composition of the maggot meal utilized in the study is detailed in Table 1. Table 2 illustrates the composition of the treatment diet, which integrated 15% maggot meal, encompassing both the control and experimental groups. The probiotics utilized in the study were sourced from the National Research and Innovation Agency (BRIN, Bogor), comprising Lactobacillus plantarum type lactic acid bacteria at a concentration of 10⁷ CFU mL^-1 in the drinking water. The treatments administered were categorized as follows: M0L0 (control feed without LAB), M0L1 (control feed with LAB), M1L0 (treatment feed without LAB), and M1L1 (treatment feed with LAB).

Chicken rearing

Chicken rearing was conducted for 63 days in the open house system. Day-old chicks (DOC) were placed in each cage, accommodating 10 chickens per cage. During the initial 14 days, commercial feed was provided and from days 14 to 63, the treatment feed was applied. The feed and the drinking water were provided ad libitum, with the volume measured before and after provision.

Chicken performance and organs

Observations of IPB D1 chicken performance involve assessing feed consumption, water intake, weight gain, and feed conversion. The relative weights of internal organs such as the proventriculus, gizzard, pancreas, small intestine, caeca, spleen, thymus, and bursa of Fabricius are also recorded. Additionally, blood profile parameters are evaluated.

Chicken health profile

Blood samples were collected from one chick per treatment group by randomly extracting 1 ml of blood from the brachial vein (located on the wing) using a syringe. The collected blood was then transferred into a vacuum container containing EDTA anticoagulant. Blood profile analysis, following the protocol outlined by Meidita et al (2020), comprised measurements of erythrocytes, hemoglobin, hematocrit, leukocytes, and leukocyte differentiation.

Data Analysis

To assess the efficacy of the four treatments, a Completely Randomized Design (CRD) with six replicates was utilized for each treatment. Subsequently, the collected data was analyzed using Analysis of Variance (ANOVA) software, specifically SPSS Statistics for Windows, Version 25.0. Upon detecting significant differences, a Tukey posthoc test was conducted to delve deeper into the variations

Results and Discussion

Chicken performance

The performance of IPB D1 chickens, encompassing feed and drink consumption, body weight gain (BWG), and Feed Conversion Ratio (FCR), is detailed in Table 3. Results indicate that the treatment involving feed supplemented with maggot meal and LAB in drinking water over the maintenance period of 2 to 9 weeks did not affect the performance of IPB D1 chickens. Similar feed consumption levels across treatments suggest that factors such as feed composition and palatability remained consistent, thereby minimizing differences in consumption rates.

Feed consumption ranged from 2243.01 to 2374.47 g chick^-1. The similarity in feed consumption across treatments can be attributed to factors such as the form of feed, nutrient composition, and consistent palatability levels. This uniformity may stem from the comparable protein content present in each feed variant. Notably, feed with high palatability tends to be consumed in larger quantities, as highlighted by Rezaei et al (2018). Hasan et al (2020) further elaborate that factors influencing feed palatability include odor and taste. Additionally, although maggot meal may initially appear less appealing to chickens due to its slightly dark color, continued exposure typically results in accustomed consumption. Despite this, feed consumption remains within acceptable limits, aligning with findings from previous studies such as that of Sinurat et al (2022), where feed consumption in Kampung chickens ranged from 2278 to 2556 g chick^-1.

Drinking water consumption ranged from 117.98 ml to 128.99 ml per chick per day, with no significant impact observed despite potential differences in water taste, which tends to be more acidic due to LAB addition. The absence of any effect of adding LAB in this study leaves questions for further investigation regarding LAB inoculants added to drinking water, including their population. As elucidated by Chen et al (2017), lactic acid bacteria play multiple roles, including lactic acid formation, enhancement of normal intestinal bacteria activity, stimulation of digestive enzyme activity, and promotion of bile salt release. These varied functions foster beneficial interactions between probiotics, resulting in a synergistic effect on feed digestion. Moreover, inter-species interactions contribute to resistance against intestinal peristalsis, rendering this bacterial blend competitive against pathogenic microbes, thereby enhancing feed processing efficacy. Consequently, Lactobacillus introduced into the chicken's digestive tract can thrive and proliferate, aiding in the enhancement of the digestive process.

Weight gain and final body weight also demonstrated no significant effect, ranging from 12.31 to 13.28 g chick^-1day^-1with the final body ranging from 828.37 - 898.92 g chick^-1. This trend corresponds to the lack of significant impact observed in feed consumption. Olejnik (2022) emphasized that body weight gain is closely tied to feed intake. Additionally, the presence of chitin in maggot meal may contribute to this phenomenon. Chitin has a propensity to form intricate bonds with nutrients, particularly proteins, rendering them indigestible in the digestive tract (Hidayat 2019). Furthermore, Nandhirabrata (2023) suggested that the addition of maggot meals had no significant effect on the feed conversion value.

The feed conversion ratio (FCR) showed no significant effect, ranging from 3.49 to 3.95. This outcome may be influenced by advancing age, which tends to diminish the efficiency of protein utilization as ration consumption increases while the increase in body weight remains relatively constant, leading to a decrease in protein efficiency. Maggot meal is recognized for its high protein content, and therefore, its inclusion in the finisher phase does not appear to impact body weight gain. Additionally, maggot meal contains chitin, which has the propensity to form complex bonds with nutrients, particularly proteins, hindering proper protein digestion in the digestive tract (Auza et al 2021). Consequently, the addition of maggot meal during the finisher phase does not seem to affect body weight gain (Pertiwi et al 2023). The FCR value achieved in this study using IPB D1 chickens showed a better value compared to that of kampong chickens (KUB breed), which reached 4.07-9.92 as reported by Sinurat et al (2020).

Blood profile

The data presented in this study (Table 4) revealed that incorporating maggot meal at levels up to 15% in the feed and supplementing LAB in drinking water during the 2- to 9-week rearing period had no significant impact on the blood profile of IPB D1 chickens. Typically, blood profile serves as an indicator of the physiological condition and nutritional status of chickens, with factors such as the quantity and nutritional quality of the feed provided known to influence blood profile (Sugiharto et al 2016).

The average values for erythrocytes ranged from 1.86 to 2.11 million ml^-1, leukocytes from 9.87 to 13.15 thousand ml^-1, hemoglobin from 8.33 to 9.53 %, hematocrit from 24.83 to 27.83%, heterophils from 39.82 to 43.97%, lymphocytes from 41.14 to 44.93%, H/L ratio from 0.92 to 1.09, eosinophils from 7.62 to 8.80%, monocytes from 5.27 to 6.15%, and basophils from 0.90 to 0.92%. The blood profile of the chickens did not exhibit significant differences, suggesting that the utilization of maggot meal and lactic acid bacteria had no discernible influence on the chickens' health parameters. Leukocytes are pivotal in the body's immune response; a low antigen content in the blood can lead to decreased antibody production (Wardiny et al 2012). The heterophil/lymphocyte (H/L) ratio serves as an indicator of stress levels in poultry. A lower H/L value signifies a lower stress level, while a higher value indicates the opposite. As per Gross and Siegel (1983), a H/L ratio of 0.2 suggests a low stress level, 0.5 denotes a normal stress level, and 0.8 signifies a high stress level. In this study, the H/L ratio fell within the category of moderate stress levels.

Vital organ

Internal vital organs, including the liver, heart, and kidneys, were assessed, with their respective percentages detailed in Table 5. Results indicated that administering feed containing maggot meal and LAB supplementation in drinking water during the 2 - 9 week maintenance period had no impact on the internal organ percentages in IPB D1 chickens.

Liver percentage ranged from 1.95% to 2.09%, heart from 0.49% to 0.54%, and kidney from 0.47% to 0.7%. This suggests that the liver functioned effectively as a detoxifier, with no observed increase in its percentage, which can be influenced by various factors including animal type, body size, genetics, and diet composition. The liver percentage observed in this study (1.95% - 2.09%) was slightly lower than that reported by Bayu et al (2022), likely due to differences in chicken breeds.

Similarly, the proportion of heart weight remained undifferent in all treatments. This suggests that the heart's development was not impacted, as blood volume and concentration remained steady or decreased due to reduced feed intake. Heart weight percentage in this study varied from 0.49% to 0.54%, consistent with the findings of Rongko (2020) in chickens fed diets containing maggot meal. In this study, heart weight percentage ranged from 0.49% to 0.54%. Consistent with research by Rongko (2020), who reported chickens fed diets containing maggot meal exhibited heart weights ranging from 0.42% to 0.59%.

Regarding kidney weight, in this study was found unaffected by the treatments. The average percentage of kidney weight ranged from 0.47% to 0.71%. According to Auza et al (2022), the normal range for kidney weight in broiler chickens is approximately 0.73% to 0.80%. The kidneys function to filter plasma from the blood, selectively reabsorb water and essential elements, and remove excess and waste products from the plasma.

Digestive organ

Table 6 illustrates the percentage of weight and length of various digestive organs as observed in the study. Findings indicate that the treatment administered during the 2 to 9-week maintenance period on IPB D1 chicken did not exert any discernible impact on the weight and length of these digestive organs. Specifically, the ventriculus accounted for 2.80% to 3.33% of the total weight, the proventriculus comprised 0.47% to 0.54%, bile constituted 0.07% to 0.73%, the pancreas ranged from 0.19% to 0.24%, total intestine made up 4.14% to 5.02%, the duodenum measured between 0.57% to 0.73%, the jejunum spanned from 0.92% to 1.30%, the ileum ranged from 0.60% to 0.86%, the cecum varied from 0.37% to 0.40%, and the colon accounted for 0.15% to 0.20%. The lengths of the duodenum, jejunum, ileum, cecum, and colon measured between 2.57 to 3.01, 5.42 to 6.31, 5.02 to 6.42, 1.23 to 1.45, and 0.82 to 0.96 cm/100 g, respectively.

In this study, the percentage of proventriculus weight did not exhibit a significant effect, as it was influenced by various other factors. Notably, the high crude fiber content in the ration had an impact. Despite the elevated crude fiber content, the proventriculus functioned relatively well. However, there were limitations each time new feed was introduced to the ration, which allowed the chicken to balance its body weight and digestion. This approach ensured that the ration did not overly strain the proventriculus, maintaining it in a normal condition (Nursiam et al 2022). Similarly, the weight of the ventriculus did not show significant differences, likely due to the high coarse fiber content in the feed. Furthermore, this high fiber content can enhance ventriculus performance, resulting in thicker ventriculus walls and affecting its function. This observation aligns with the assertion of Nursiam et al (2022) that increased crude fiber in the ration reduces small intestine thickness but increases muscle mass in the proventriculus and ventriculus. Moreover, ventricle weight can increase with higher crude fiber content in the diet, leading to heightened contractions during the digestion of crude fiber (Bayu et al 2022).

The small intestine is comprised of three segments: the duodenum, jejunum, and ileum. Collectively, the small intestine serves as the primary site for food absorption (Ravindran and Abdollahi 2021). The duodenum is responsible for breaking down nutrients from the feed, while the jejunum serves as a site for further absorption of nutrients previously processed by the duodenum. The ileum functions to absorb water and minerals.

The results of the analysis of variance indicated variations in the average values of both the percentage and length of the duodenum. The highest percentage and length of the duodenum were observed in M1L1 (treatment feed with LAB) at 0.73% and 3.01 cm/100 g, respectively. Differences in duodenal percentage are attributed to variations in crude fiber content within the diet. The elevation of crude fiber in the ration may be influenced by the high crude fiber content present in maggot meal. Elevated crude fiber accelerates the rate of digestion, leading to a reduction in the available time for digestive enzymes to thoroughly degrade nutrients, consequently decreasing nutrient digestibility (Prawitasari et al 2012).

Therefore, to optimize the absorption of these food substances, it becomes necessary to expand or lengthen the absorption area. This aligns with the assertion of Mistiani et al (2020), who suggest that higher levels of crude fiber in the feed ration prompt expansion or elongation of the small intestine, resulting in a greater percentage of the small intestine.

The highest percentage values for both the jejunum and ileum were observed in M0L0 (control feed without LAB) at 1.29% and 0.86%, respectively. In line with this, the greatest relative length of the jejunum and ileum was recorded at 6.31 cm/100 g and 6.42 cm/100 g. According to Agriani et al (2022), the relative weight of the jejunum typically ranges between 1.77% to 1.85% or from 8.88 to 9.02 cm/100 g, while the weight of the ileum ranges from 1.60% to 1.72% or 8.89 to 9.01 cm/100 g, respectively. These findings indicate that the percentages and relative lengths of the jejunum and ileum remain within normal ranges, suggesting that the addition of maggot meal as a source of protein and fat has no adverse effects on these parameters.

In terms of cecum length, the research results indicated that the inclusion of maggot meal in the rations did not impact the percentage or relative length of the cecum. The highest percentage value was recorded in the control feed without LAB (M0L0) at 0.40% or 1.45 cm/100 g. Incorporating maggot meal as a protein and fat source did not adversely affect the cecum. The cecum serves as a site for microbial digestion to break down nutrients that remain unabsorbed by the intestine (Ravindran and Abdollahi 2021). Within the cecum, microbes are capable of digesting crude fiber, converting it into volatile fatty acids used to meet the organ's energy demands. Increased feed consumption leads to heightened digestive tract activity, thereby stimulating the growth of digestive organs (Wang et al 2020).

The colon, a component of the large intestine, regulates water balance and absorbs nutrients that escape digestion in the small intestine (Hidayati et al 2019). The addition of maggot meal did not affect the relative length and weight of the colon. The highest percentage weight and relative length values were observed in M1L1 (treatment feed with LAB) at 0.20% and 0.96 cm/100g, respectively. The weight and length of the colon can be influenced by the crude fiber content in the diet. Maggot meal supplementation contains 4.46% crude fiber, higher than other treatments. According to Sasae et al (2020), a high crude fiber content in feed can increase water consumption, potentially leading to an increase in colon percentage.

Immune organs

The research analysis results indicated that administering maggot meal and LAB supplementation in drinking water during the 2nd to 9th week of maintenance did not exhibit an effect on the immune organs of IPB D1 chickens. The average weight percentage of the spleen ranged from 0.15% to 0.35%, thymus from 0.378% to 0.435%, and bursa from 0.035% to 0.048%. According to Nandhirabrata (2023), lymphoid organs, such as the thymus, bursa Fabricius, and spleen, play crucial roles in maintaining the immune system by housing lymphocytes. A decrease in the weight of lymphoid organs may result in lower antibody production by lymphocytes. Additionally, Ridla et al (2023) reported that exogenous enzyme addition and feed digestibility increased the relative weight of the lymphoid organs, including the thymus, bursa Fabricius, and spleen.

Carcass yield

The carcass quality of IPB D1 chickens is summarized in Table 8. According to the research findings, none of the treatments affected the quality of IPB D1 chicken carcass yield. The average percentages of carcass yield ranged from 62.34% to 64.88%, chick and neck from 9.3% to 9.78%, back from 12.53% to 14.7%, chest from 14.98% to 15.62%, wings from 8.98% to 9.81%, upper thighs from 11.12% to 11.64%, lower thighs from 10.6% to 11.4%, and legs from 4.54% to 4.97%.

Differences in carcass weight can be attributed to variations in nutritional composition among the different treatment feeds. The protein content in rations significantly influences the attainment of livestock body weight, as reported by Usturoi (2023). One of the key factors influencing the growth of carcass tissue in broiler chickens is their diet, which provides essential nutrients for growth. If the nutrients supplied are inadequate, the growth of broiler chickens may be hindered, subsequently affecting their overall carcass weight. According to Hafid (2023), the growth coefficient of male and female broiler carcasses was the same, indicating they undergo a similar early development phase compared to the growth of the body as a whole. As a result, the growth and development patterns of the carcasses of both male and female broiler chickens at the age of 0 to 5 weeks were relatively similar.

Conclusion

Incorporating 15% maggot meal into the feed and supplementing with lactic acid bacteria in drinking water does not adversely affect the growth performance or health status of IPB D1 chickens. Consequently, maggot meal emerges as a promising alternative protein source for feeding IPB D1 chickens. Further research is essential to investigate additional parameters for evaluating chicken health and to establish the optimal dosage limit for integrating maggot meals into the diet of IPB D1 chickens.

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