Additive effects of Bridelia ferruginea leaf meal as a partial replacement for soybean meal on nutrients digestibility, growth performance, and carcass characteristics of weaner rabbits

Abstract

Background

Protein is a crucial nutrient for enhancing livestock performance and productivity, traditionally sourced from soybean and fish meal. However, issues like erratic availability and rising prices necessitate exploring alternative protein sources. Tropical plants, especially leaf meals, are being considered to replace or supplement conventional protein sources in rabbit diets. Bridelia ferruginea, a plant abundant in West Africa, is recognized for its medicinal properties, but its potential as an animal feed is largely unexplored. This study aims to evaluate the impact of graded levels of Bridelia ferruginea leaf meal (BFLM) as a partial substitute for soybean meal in the diets of weaner rabbits.

Materials and methods

The experiment was conducted at the Animal Science Department of Kwame Nkrumah University of Science and Technology in Ghana. BFLM was obtained by air-drying harvested leaves and milling them. Four diets were formulated, with BFLM partially replacing soybean meal at levels of 0%, 10%, 20%, and 30%. Representative samples of BFLM and all formulated diets were analyzed for their proximate composition and detergent fibre fractions. Twenty-four weaner rabbits were assigned to these diets in a Completely Randomized Design. The study covered a 10-week period, assessing growth performance, nutrient digestibility, carcass characteristics, and economics of production.

Results

The chemical composition of BFLM revealed favorable attributes for rabbit feeding, with 20.5% crude protein and 92.6% dry matter. Growth performance declined at 30% BFLM inclusion, indicating a possible impact of anti-nutritional factors. Feed conversion ratio increased at higher BFLM levels. Nutrient digestibility showed a decline in dry matter digestibility at 30% BFLM. Carcass characteristics were affected at higher BFLM levels, with dressing percentage decreasing. Weights of internal organs were generally not negatively affected by the inclusion of BFLM. Economic analysis indicated a linear reduction in feed cost with increasing BFLM inclusion.

Conclusion

The study suggests that BFLM can be incorporated up to 20% in weaner rabbit diets without compromising productivity, nutrient digestibility, or dressing percentage. Beyond 20%, adverse effects on growth performance and some carcass characteristics were observed. Economically, BFLM incorporation up to 20% lowered feed costs without compromising feed efficiency. Incorporation of BFLM up to 20% in weaner rabbit diets had no adverse effects on the weights and functions of the heart, liver, and kidneys. Overall, BFLM presents a promising alternative protein source for weaner rabbit diets, contributing to cost-effective and sustainable livestock production.

Background

Protein is an essential nutrient for improving the performance and productivity of livestock. Traditionally, protein sources such as soybean meal and fish meal have been widely used successfully. However, in addition to their erratic availability, the prices of these protein sources continue to rise. Tropical plants are usually available throughout the year because of their rapid growth, which is enhanced by the prevailing environmental factors. As a result, using leaf meals to replace soybean meal, either whole or partially, in the diets of rabbits has received considerable attention (Amata and Bratte 2008; Oloruntola et al. 2018; Jiwuba and Ogbuewu 2019; Osman et al. 2022).

It is in light of this that the use of plants in different forms as alternatives to the relatively expensive and scarce conventional feed resources in livestock production is becoming more popular in the tropics. This is because these plants and their parts have been reported to serve as a crucial source of protein, phytobiotics, and antioxidants (Oloruntola et al. 2018). The inclusion of tropical leaves in the form of leaf meals in the diet is capable of reducing the cost of commercial feeds, with a resultant reduction in the cost of animal protein and improvement in animal health (Oloruntola et al. 2018). Additionally, the rapid increases in human and livestock populations have resulted in increased food and feed needs in developing countries, necessitating the identification and evaluation of alternative feed supplies (Odunsi et al. 2002).

Bridelia ferruginea is a small, non-lactiferous scaly tree or shrub that is common in Guinea and Mali, as well as in South Nigeria and throughout the wooded savanna regions of Africa. It is a straggly tree about 15 m tall with a crooked trunk up to 1.80 m in circumference. It is mostly found in savanna forests and open coastal plains, as well as, at times, on rocky soils (Ameyaw et al. 2012). B. Ferruginea is widely cultivated in West African countries such as Mali, Nigeria, Ghana, and Sierra Leone, among others. The Bridelia plant is readily available in Ghana, where it is mostly used for the management of diabetes mellitus and hypertension (Alowanou et al. 2015). The leaves are also fed to small ruminants (Onwuka 1994), particularly in the dry season when grass is scarce and of poor quality. This is because leaves of B. ferruginea remain green even during the dry season and could serve as a cheap supplementary feed resource for ruminants and non-ruminant herbivores. The leaves have been reported by Sasu et al. (2023) to contain 194.0, 155.5, 301.9, 478.5 and 429.3 g/kgDM of crude protein, ash, crude fibre, neutral detergent fibre and acid detergent fibre in that order. This makes B. ferruginea a potentially good resource as livestock feed. Even though the ethnomedicinal, phytochemical, pharmacological, and toxicological properties of B. Ferruginea has been widely studied (Yeboah et al. 2022), but information regarding the use of the leaves as animal feed, in terms of acceptance, tolerance and digestibility, is scanty. It is hypothesized that B. ferruginea leaves can be a cost-effective and readily available alternative protein source to soybean meal for weaner rabbits in Ghana, without negatively impacting their growth performance, nutrient digestibility, carcass characteristics, or organ weights.

This study sought to evaluate the response of weaner rabbits to graded levels of B. ferruginea leaf meal (BFLM) as a partial replacement for soybean meal. Rabbits were chosen as models for ruminants in view of their ability to handle high fibre present in BFLM. Again, when rabbit production is given the needed attention and reared on a commercial basis, it could solve the problem of low animal protein intake in the developing world as they are prolific and grow fast (Osman et al. 2020). Specifically, the study sought to determine the growth performance and economics of production, apparent nutrients’ digestibility, carcass characteristics and organ weights of weaner rabbits fed diets containing varying levels of BFLM.

Materials and methods

Location of experiment

The study was conducted at the Animal Science Department of Kwame Nkrumah University of Science and Technology (KNUST), Kumasi, Ghana. The department is located in the south-eastern part of Kumasi. The annual monthly temperatures of the area vary between 26.1 and 28.9 ℃. High temperatures occur during the months of November to April, with maximum temperatures occurring between February and March, while the lowest temperature is experienced in July. Rainfall in the area is bimodal, with an annual mean of 1500 mm (Weather Spark 2022).

Harvesting and processing of B. ferruginea leaf meal

Fresh leaves of B. ferruginea were harvested from mature trees at the Department of Animal Science, KNUST. The harvested leaves were then detached from the stems and air-dried in a well-ventilated shed for 14 days until they were crispy to touch while still green. After air drying, the leaves were milled using a hammer mill with a sieve size of 2 mm to produce the B. ferruginea leaf meal (BFLM). Analysed chemical composition of B. ferruginea is presented in Table 1.

Table 1 Chemical composition and metabolisable energy content of air-dried BFLM

Feed ingredients and experimental diets

Soybean meal, wheat bran, dicalcium phosphate, and vitamin premix were procured from a commercial feed supplier, while the millet mash residue was obtained freely from local porridge sellers in Kumasi in the wet state and then sun-dried for 3–5 days. Millet mash residue is the residue left when a mixture of millet dough or flour and water is sieved during the preparation of millet porridge.

Four experimental diets were formulated. The corresponding dietary treatments were designated as 0%BFLM (the control diet, which contained soybean meal as the main source of protein), 10%BFLM, 20%BFLM, and 30%BFLM, which contained 10, 20, and 30% BFLM, respectively as partial replacements for soybean meal. The diets and water were fed to the rabbits in the different treatment groups ad libitum for 10 weeks. Details of the inclusion levels of ingredients and the chemical composition of the formulated diets are shown in Table 2. The crude protein contents were within the 18–22% reported by Akande (2015) to be optimum for the production of tropical rabbits.

Table 2 Percentage inclusion levels of dietary ingredients in diets and analysed chemical composition of diets

Experimental animals and management

Twenty-four (24) unsexed weaner rabbits of mixed breeds (from New Zealand White and Californian breeds) aged 6 weeks and weighing between 760 and 790 g were used. They were housed individually in two-tier wooden cages with welded-mesh floors. Each animal was provided with an earthenware feeder and drinker specifically designed to reduce spillage. They were assigned to the four dietary treatments with six animals per treatment in a completely randomized design (CRD) experiment. Each treatment was replicated six times. Each rabbit was fed the assigned diet for 10 weeks after a 1-week adjustment period. Before the study began, each animal was dewormed using Piperazine (Dorpharma B.V. Limited, The Netherlands). Coccidiostat was also administered continuously for 3 days as a preventive measure against coccidiosis using Britacox (Special T Products Limited, United Kingdom).

Animal care and welfare

Ethical approval was sought from Animal Research Ethics Committee (AREC, 2018) of the Quality Assurance and Planning Unit of KNUST (Approval number: KNUST 0027). All necessary standard operating procedures outlined by AREC (2018) were followed.

Growth study and economics of production

The rabbits were fed and provided with water individually in separate earthenware feeders and waterers at 8:00 a.m. Each rabbit’s daily feed intake was 10% of its body weight. All rabbits were weighed at the start of the study before being allotted to the various treatments. Growth performance parameters measured were average feed intake (total feed intake divided by the number of days the rabbits were fed), live weight changes (total weight gain: final weight minus initial weight; average daily gain: final weight minus initial weight divided by number of days the rabbits were fed), and feed conversion ratio (average daily feed intake divided by average daily gain). Feed cost per kilogram diet and feed cost per kilogram of weight gain (product of the feed cost per kg diet and feed conversion ratio) were also calculated for the determination of the economics of production.

Digestibility study

A digestibility study was undertaken during the 6th week of the feeding and growth trial, which involved feeding the rabbits with known quantities of feed. Total feces were collected daily and oven-dried to determine moisture content. The digestibility values for dry matter (DM), crude protein (CP), crude fiber (CF), crude fat, ash, neutral detergent fiber (NDF), and acid detergent fiber (ADF) were calculated as nutrient intake minus nutrient excreted divided by nutrient intake multiplied by 100 (Perez et al. 1995).

Evaluation of carcass characteristics

At the end of the 10-week trial, three rabbits per treatment were randomly selected, starved of feed and water for 12 h, and humanely slaughtered. Blood weight was estimated as the difference between live slaughter weight and hot carcass weight. The carcasses were defurred using flame and eviscerated to evaluate their carcasses. Dressing percentage was determined by dividing the hot-dressed carcass weight by the slaughter weight and multiplying by 100 according to the procedure of Gugolek et al. (2011). The weights of the gastrointestinal tract (full and empty), liver, kidney, lung, heart, and caecum (full and empty) were measured as described by Jiwuba and Ogbuewu (2019).

Economics of production

Market prices for the various feed ingredients (Table 3) were used for the economic appraisal of the feeds, which was based on the feed cost per kg diet and feed cost per kg weight gain. Feed cost per kg of live weight gain was calculated as a product of the feed cost per kg of diet and feed conversion ratio for individual dietary treatments.

Table 3 Feed ingredients and their prevailing prices per kilogramme used for the economic appraisal of the feed

Chemical analyses of BFLM and experimental diets

Representative samples of BFLM, all formulated diets and dried feces were analyzed for their proximate composition according to the procedures of AOAC (2005). NDF and ADF fractions were determined following the technique described by Goering and Van Soest (1970).

Statistical analysis

The data collected from the feeding trial, digestibility study, and carcass yield evaluations were subjected to analysis of variance (ANOVA) using Minitab Version 18.1. The means were separated by Tukey’s post-hoc test. The probability level of significance was set at 5%.

Results

Growth performance of rabbits fed the formulated diets

Growth performance indices of weaner rabbits over the 10-week period and economic appraisal of the experimental diets formulated are shown in Table 4. The initial body weights and average daily feed intake of the weaner rabbits were similar (p > 0.05). Final weight gain, total weight gain, and average daily gain (ADG) declined significantly when BFLM was increased to 30% even though daily feed intake among the various treatments were similar. Feed conversion ratio (FCR) for 10%BFLM and 20%BFLM were similar to that of the BFLM-free control diet but declined significantly when BFLM was increased to 30%. Both feed cost/kg and feed cost/kg gain declined linearly with increase in the inclusion level of BFLM.

Table 4 Productive performance of weaner rabbits fed the experimental diets

Effects of feeding BFLM on nutrients digestibility of weaner rabbits

The effects of feeding diets containing graded levels of BFLM on apparent nutrient digestibility coefficients of weaner rabbits are presented in Table 5. The results showed differences (p < 0.05) in digestibility coefficients for all nutrients considered but for CP. DM digestibility ranged from 56.87% in 30%BFLM to 61.97% in 20%BFLM. Thus DM digestibility declined when BFLM was increased to 30% in the diet. Digestibility coefficients for ether extract followed a similar trend. Crude fibre digestibility significantly increased when the inclusion level of BFLM was increased to 30%. However, digestibility coefficients for ash, NDF, and ADF differed significantly from the control BFLM-free diet when BFLM was increased to 20%. The said coefficients were similar for 20%BFLM and 30%BFLM.

Table 5 Apparent nutrients digestibility of grower rabbits fed the experimental diets

Effects of feeding BFLM on carcass characteristics of grower rabbits

Live slaughter weight, carcass, and organ characteristics of rabbits fed BFLM are presented in Table 6. Significant differences (p < 0.05) were observed as a result of treatment effects for live slaughter weight and all carcass parameters, with the exception of the weights of the liver, kidney, and heart. Dressed weight, dressing percentage, and full and empty GIT weights decreased linearly with increase in the inclusion level of BFLM. Lung weight was significantly lower in 30%BFLM. However, weights of both full and empty caeca were highest in 30%BFLM and lowest in the BFLM-free control diet.

Table 6 Carcass characteristics of grower rabbits fed the experimental diets

Discussion

Chemical composition of air-dried BFLM presented in Table 1 showed that BFLM was well-dried (DM; 92.6%), fibrous (NDF; 40.5%), and high in CP (20.5%), rendering it appropriate for feeding rabbits. The current CP value for BFLM was higher than the 15.57% reported by Onwuka (1994) for B. ferruginea leaves as well as the 15.7% reported by Jonathan and Funmilola (2014) for the stem bark of B. ferruginea. The inequalities in CP contents relative to those of earlier works may be attributed to the age at harvesting, the prevailing climatic conditions, soil factors, and methods employed in the processing and analysis of leaf samples (Fuglie, 1999). The chemical components of BFLM looked good compared to other leaf meals that have been successfully utilized in rabbit diets. The CP content was higher than 19.5% of Paper mulberry leaves (Osman et al. 2022), 17.0% of Ackee leaves (Osman et al. 2020), and 15.6% of Gliricidia leaves (Amata and Bratte 2008), but lower than 28.2% of Moringa leaves (Tesfaye et al. 2013). BFLM had similar CP values to Leucaena leucocephala, as reported by Safwat et al. (2015). The crude fiber content of BFLM was higher than that of all the aforementioned leaves, with the exception of Ackee leaves, which had similar values. In contrast, the ash content of BFLM was lower relative to that of the other leaves, with the exception of Ackee leaves, where once again the values were similar.

The control diet recorded the highest CP content (21.9%), undoubtedly due to the highest inclusion level of soybean meal. The contents of crude fiber and fat increased linearly with an increase in the inclusion level of BFLM. The fiber contents of the experimental diets were generally lower than the 14–18% on a dry matter basis recommended by Gidenne and Lebas (2002). The metabolisable energy (ME) contents of the experimental diets were all within the range of values reported by Njidda and Isidahomen (2010) and Osman et al. (2022), but lower than those found by Osman et al. (2020). All the formulated diets, however, generally met the minimum nutrient requirement for rabbits, as published by Maertens (1992).

The absence of differences in feed intake is consistent with the findings of Oloruntola et al. (2018) but at variance with those of Jiwuba and Ogbuewu (2019), who reported differences in feed intake when soybean meal was replaced with Moringa oleifera leaf meal. Live body weight changes, feed conversion ratio, and feed cost/kg gain were, however, affected (p < 0.05) by treatment effects. The decline in live weight changes and FCR observed relative to the 30% inclusion level could be due to anti-nutritive factors like phenolics, phytosterols, tannins, flavonoids, saponins, and alkaloids reported to be present in B. ferruginea by Ndukwe et al. (2007) and Abubakar et al. (2018) that may have bound the nutrients in the feed and reduced their bioavailability and utilization.

ADG declined with increase in level of BFLM probably due to the decline in CP and ME contents of the diets (Table 2) even though all diets met the minimum nutrient requirements for rabbits as stated earlier. The decline could also be linked to the presence of antinutritional factors like phenolics, tannins, flavonoids, saponins, alkaloids etc. present in BFLM (Ndukwe et al. 2007) that influence bioavailability of nutrients at high levels. The present ADG values (11.14–13.26 g) were higher than the 8.93–10.57 g reported by Osman et al. (2020) but lower than the 16.79–21.9 g and 31.13–34.03 g reported by Jiwuba and Ogbuewu (2019) and Oloruntola et al. (2018) respectively. The differences between ADG values in the present study and those of earlier works could be attributed to the different levels of different leaf meals and ingredients used in compounding the diets. The differences in FCR observed due to treatment effects were inconsistent with the report of Oloruntola et al. (2018) but in line with the findings of Jiwuba and Ogbuewau (2019) and Osman et al. (2020). The present values for FCR (5.28–6.27) were higher (poorer) than the 2.39–2.53 reported by Oloruntola et al. (2018) and the 4.00–4.74 recounted by Jiwuba and Ogbuewu (2019), but well within the range of 5.5–6.3 reported by Osman et al. (2022). Feed cost per kilogram and per kilogram gain both declined linearly (p < 0.05) with an increase in the inclusion level of BFLM. The decline in feed cost per kilogram was due to the low cost of BFLM, which has highlighted the economic benefits of the addition of BFLM to the diet. This trend is also consistent with the findings of Ogundipe et al. (2014) and Osman et al. (2022).

It is noteworthy that dry matter digestibility declined when the inclusion level of BFLM was increased to 30%. This could also be attributable to the effects of antinutritional factors (phenolics, phytosterols, cardiac glycosides, triterpenes, tannins, flavonoids, saponins, and alkaloids) present in the leaves (Abubakar et al. 2018; Cimanga et al. 2001; Ndukwe et al. 2007) that may have reduced the bioavailability of nutrients at that high inclusion level.

Digestibility values for dry matter in the present work (56.87–61.40%) were lower than those of earlier work (67.55–74.94, 75.67–82.33, and 78.26–83.51% by Eustace and Oluwakemi (2003), Bamikole et al. (2005), and Ajayi et al. (2007), respectively). The present digestibility coefficients were, however, higher than the 52.3–57.7% reported by Dougnon et al. (2012). The CP digestibility coefficients of the leaf meal-based diets were compared favorably with those of the control diet, suggesting that BFLM could be utilized at varying levels up to 30% without any adverse effect on CP digestibility. The present CP digestibility coefficients (62.67–64.17%) were comparable to the 59.0–74.0% recounted by Iyeghe-Erakpotobor et al. (2006) but lower than the 76.33–84.0% reported by Bamikole et al. (2005). Fibre digestibility significantly (p < 0.05) improved linearly as the inclusion level of BFLM in the diets increased, probably due to the rapid passage of feed through the gastrointestinal tract (Gidenne, 2000) with the inclusion of BFLM. Values for fiber digestibility in the present study (60.38–68.16%) were lower than the 79.67–88.67% reported by Bamikole et al. (2005) but comparable to 63.85–68.88% obtained by Osman et al. (2020). The present values were, however, higher than the 33.37–48.53% and 50.01–55.0% reported by Iyayi and Odueso (2003) and Iyeghe-Erakpotobor et al. (2006), respectively. Digestibility coefficients for NDF and ADF followed a trend similar to that of crude fiber. The values increased (p < 0.05) linearly with an increase in the inclusion levels of BFLM, but the values for the BFLM-based diets were similar. The differences in NDF and ADF digestibility contradicted the findings of Osman et al. (2022), who found no differences in digestibility when paper mulberry leaf meal was incorporated in rabbit diets, as well as the results of Safwat et al. (2015), who reported a rather higher digestibility coefficient for the control diet relative to leaf meal-based diets. The current values for fat digestibility (58.76–71.40%) were all lower than the 88.03–90.66% and 80.01–81.90% reported by Iyayi and Odueso (2003) and Oso et al. (2006), respectively, but within the range of 55.65–86.0% recounted by Bamikole et al. (2005). Ash digestibility also increased (p < 0.05) linearly when the inclusion level of BFLM was increased from 0 to 30%. However, the present range of digestibility coefficients (28.95–41.53%) was lower than the ranges of 52.0–62.67% and 75.11–86.43% reported by Bamikole et al. (2005) and Ajayi et al. (2007), respectively.

Dressing percentage significantly (p < 0.05) decreased beyond the 20% inclusion level of BFLM, which could be attributed to the presence of anti-nutritional factors present in the leaves that may have hindered growth or weight gain as stated earlier relative to the other inclusion levels. This trend was contrary to the reports of Omole et al. (2007) and Amata (2010) when Stylosanthes guianensis/Lablab purpureus and Gliricidia leaf meal, respectively, were fed to rabbits. The current values for dressing percentage (58.5–63.97%) were, however, higher than the 49.4–56.4% reported by Adeosun and Iyeghe-Erakpotobor (2012) and within the range of 58.4–67.2% reported by Akinmoladun et al. (2018). Weights of internal organs like the heart, kidney, and liver are commonly used in feeding trials to determine whether nutritional interventions have negative effects on animals (Ahamefule et al. 2006; Ngi (2012). Based on the comparability of the weights of the internal organs across the various treatments, the inclusion of BFLM did not appear to have any adverse effects on the internal organs. This observation was in line with the findings of Oloruntola et al. (2015) but contradicted the results of Akinmoladun et al. (2018), who observed differences in the weights of the aforementioned organs. The weight of the lungs, however, decreased significantly when BFLM was increased to 30%. Weights of full and empty caeca increased linearly with an increase in the inclusion level of BFLM, probably due to the accompanying increment in fiber levels of the diets. This observation agreed with the work of Chao and Li (2008), who reported an increase in the weight of caecum when the dietary fiber level was increased.

Conclusions

The results of the present study suggest that BFLM could be incorporated into the diet of weaner rabbits as a partial replacement for soybean meal up to 20% without negatively affecting intake of feed, weight gain, FCR, nutrient digestibility, or dressing percentage. BFLM could be utilized up to 20% to lower the feed cost in the diet of weaner rabbits without compromising productivity. As a final point, dietary incorporation of BFLM up to 20% in weaner rabbit diets had no adverse effects on the weights and functions of the heart, liver, and kidneys.

Recommendation for further research

Further research into the effects of BFLM on blood parameters and meat quality is essential to fully comprehend its potential benefits and applications in rabbit nutrition. This knowledge will support informed decisions regarding BFLM supplementation, promoting healthier rabbit production and higher quality meat for that matter.