Reviews in Agricultural Science
Online ISSN : 2187-090X
Feeding Fermented Agricultural Byproducts as a Potential Approach to Reduce Carbon Footprint from Broiler Production – A Brief Overview
Sugiharto Sugiharto
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2022 Volume 10 Pages 90-100

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Abstract

Agricultural activities have been connected to greenhouse gasses (GHG) emissions, with carbon dioxide, nitrous oxide and methane being the most GHGs emitted. Despite the fact that broiler production produces less GHG than other animal production farms, the broiler farm does emit GHG, with feed production and broiler excreta handling accounting for the majority of the emissions. It has been confirmed that fermenting and using agricultural byproducts as broiler feed ingredients reduces the use of energy- and protein-rich diets, and so reduces the carbon footprint. Feeding fermented agricultural byproducts to broilers improves feed digestibility and nutrient utilization (especially protein), hence reducing nitrogen excretion as a source of nitrous oxide. This review article provides a brief overview on the role of fermentation in improving the nutritional properties of agricultural byproducts and their use in diets to reduce the carbon footprint of broiler production.

1. Introduction

The broiler industry has grown tremendously in the last two decades in Indonesia and worldwide. The broiler industry not only helps to supply the community’s protein demands, but also contributes significantly to the Indonesian economy. Aside from economics point of view, carbon footprint is now a major environmental concern all over the world. In general, carbon footprint is referred as the total amount of greenhouse gases (GHG; including carbon dioxide [CO2], methane [CH4] and nitrous oxide [N2O]) produced by anthropogenic activities [1]. The Indonesian government now encourages a green economy that has no negative environmental impact [2]. On this spirit, all industrial sectors in the country are expected to implement the principles of green industry for sustainable economy growth and development. In this case, economic growth must be proportional to GHG reduction. Agriculture has been linked to GHG emissions, with nitrogen oxide and methane being the most common GHG emitted by agricultural activities [3, 4]. Despite the fact that GHG emissions from chicken production farms are low in comparison to other animal production farms, the broiler industry does produce GHG through feed production, fossil fuel use, and manure management [3]. Indeed, the broiler industry cannot be separated from the role of other supporting industries, such as feed industry, housing facilities and infrastructure, transportation and others that may produce GHG.

In broiler production, feed production accounted for the major sources (78%) of GHG emissions, in addition to the direct energy usage on farms, post-farm meat processing and transportation and manure storage and processing [1]. Since feed production generates the highest GHG, the efficiency by which broilers convert feed into meat is therefore a critical factor of emission intensity in broiler production [1, 3]. Fermentation has long been known as a simple method to improve the nutritional qualities of feeds or feed ingredients for broilers [5]. In this respect, fermentation could be employed to turn inexpensive and plentiful agricultural byproducts into feasible alternative feed materials for broiler production. It has been confirmed that feeding fermented feed is associated with the improved feed digestibility and reduced ammonia (source of nitrous oxide) emissions [6]. In this regards, the use of fermented agricultural byproducts as feed ingredients may help to reduce GHG production from broiler industry. Fermentation may also reduce the decomposition of organic waste (agricultural byproducts) that can increase methane emission.

Studies on the use of fermented agricultural byproducts to reduce the proportion of energy- and protein- rich feed ingredients in broiler diets are abundant [7, 8, 9, 10, 11, 12]. However, study overviewing the potential of feeding fermented agricultural byproducts to reduce carbon footprint in broiler production is still lacking. This review article aimed to provide a brief overview of how to use fermentation to improve the nutritional properties of agricultural byproducts and their use in diets to reduce the carbon footprint of broiler production.

2. Carbon footprint of broiler production

The term carbon footprint is now commonly used as a shorthand for the quantity of carbon emitted by an anthropogenic activity. MacLeod et al. [1] defined carbon footprint as the overall quantity of GHG emissions connected with a product, including emissions from consumption, end-of-life recovery, and disposal. The carbon footprint is usually presented in kilograms or tonnes of carbon dioxide equivalent (CO2-eq). Carbon emission, as the GHG with the highest amounts of emissions in the atmosphere, have a huge impact on the world. The GHG emission leads to global warming and, eventually, climate change. On a worldwide basis, agriculture is responsible for 20% of anthropogenic GHG [4, 13]. Fuel consumption, land use change, soil cultivation, and nitrous oxide emissions are the most significant sources of agricultural GHG, whereas animal waste and enteric fermentation are the most significant GHG from farm animal production [13]. Chickens are predicted to emit 0.6 gigatonnes CO2-eq, accounting for 8% of all emissions from the livestock sector. With regard particularly to broiler production, GHG emissions were accounted for by 78% of feed production, 8% by direct energy use on farms, 7% by post-farm meat processing and transportation, and 6% by manure storage and processing [1]. In relation to farm operations (on-farm activities), carbon dioxide, methane, and nitrous oxide have been recognized as the primary sources of GHG emissions. Study in Malaysia by Suffian et al. [14] specifically revealed that manure produced the most carbon dioxide equivalent, while feed produced the most methane equivalent. In the commercial modern broiler farm, bedding produced the most nitrous oxide emissions.

Protein is a key component of broiler feed, which is primarily made up of soybean meal. Indeed, the growth in broiler industry elevates the demand for soybean meal and eventually increase the soybean production. Given that the protein production system is a source of GHG emissions, land use change as a result of soybean expansion and cultivation can result in large GHG emissions. Indeed, nitrous oxide emissions have a significant influence in GHG emissions from soybean cultivation [15]. Energy, in addition to protein, is an important component of broiler diets. Yellow maize is generally considered as the primary energy source for broilers. More than half of the dietary components for broiler chickens come from this grain. In line with soybean, cultivation of maize is also attributed to the GHG emission. In this case, land preparation, sowing, fertilizer application, irrigation, pest management, and other management activities have a substantial impact on the emission of carbon dioxide and nitrous oxide from maize cultivation [4].

3. Fermentation as a method to improve nutritional quality of agricultural byproducts

Currently, the demand for feed is rising along with the growing of broiler industry. Such increased feed demand may result in higher market prices for these certain feed ingredients, particularly soybean meal (protein rich feed component) and maize (energy rich feed component). In response to this condition, farmers will generally increase soybean and corn production to satisfy market demand, which unfortunately will increase the carbon footprint. In most countries, including Indonesia, agricultural activities produce massive amounts of byproducts, which may pollute the environment if they are not adequately treated. Agricultural leftovers from crop, fruit, and vegetable processing have recently attracted the interest of animal nutritionists as an alternative feed source. In a meta-analysis of the environmental implications of agricultural production systems, Clark and Tilman [16] discovered that using agricultural wastes and byproducts as animal feeds can lower the environmental impacts of livestock production by 20%. In this regard, using agricultural byproducts as animal feeds may assist to reduce pollution caused by GHG released during the decomposition of organic waste [17]. In terms of broiler diets, there are some examples of agricultural byproducts that can be used for alternative feed ingredients, including wheat bran, cottonseed meal, cottonseed cake, groundnut cake, palm kernel meal, palm kernel cake, copra meal, coconut dregs, banana peel meal, soybean hull, brewers grains (dried and bran), rice bran, rice husk, rice chaff, cassava pulp, cassava peeling, orange peels and pulp, and maize bran [7, 9, 12, 18]. These agricultural byproducts are abundant and available all year, so using them as the alternative feed source can help broilers become less reliant on conventional feed ingredients while also lowering feed costs. Apart from their potential, the use of agricultural byproducts as an alternative feed item for broiler chicks is frequently limited due to the low quality of feed materials, variances in feed ingredients, and the presence of antinutrients, toxins, and pollutants in agricultural byproducts. Zhang et al. [19] have recently confirmed that agricultural byproducts contain significant amounts of non-starch polysaccharides that cannot be digested and utilized by broilers as the animal lack of endogenous hydrolysing enzymes. In this context, the soluble non-starch polysaccharides may increase digesta viscosity and thus reduce nutrient digestibility in the small intestine of chicken.

Fermentation is a simple technique for preserving and improving food qualities that has been practiced by our ancestors for centuries. In general, fermentation can be defined as a dynamic process that converts complex substrates into simpler molecules by involving microbes and substrates. Some factors may influence the fermentation process and fermented products, including temperature, the microbes used as starters, the nature and composition of the medium, pH, dissolved oxygen and carbon dioxide, operational systems (e.g., batch, fed-batch, continuous), addition of precursors, mixing (cycling through varying environments) and fermenter shear rates, and the length of the fermentation [5]. Other than for foods, fermentation has been applied in feed industry to improve the nutritional contents of feeds or feed components, particularly to increase crude protein and decrease fibre contents [20, 21]. Fermentation may also reduce the contents of antinutrients, toxins, and pollutants in the substrates. These features are essential for turning the agricultural byproducts to alternative feed ingredients for broilers [5, 21]. Table 1 shows some studies showing the efficacy of fermentation in improving the nutritional values and reducing the antinutrients in agricultural byproducts.

Table 1: Examples of fermentation and its effect on nutritional values of agricultural byproducts
Agricultural byproducts Fermentation starter Effect of fermentation References
Cottonseed meal B. subtilis ST-141 and Saccharomycetes N5 Decreased free gossypol level, and increased acid-soluble protein level [22]
Rice bran Aspergillus flavus PHY168 Decreased dry matter and fibre, while increasing crude protein, ether extract, ash and phosphorus contents [23]
Rice bran Bacillus amyloliquefaciens Reduced fibre content and increased total protein and gross energy [24]
Copra meal S. cerevisiae (and mannanase) Increased protein, amino acid content (especially lysine), while decreasing fibre content [25]
Coconut dregs S. cerevisiae Increased protein and decreased fibre contents [11,12]
Cassava pulp Ch. Crassa and B. subtilis (two-stage fermentation) Increased fat, crude protein and metabolizable energy, while decreasing crude fibre contents [8]
Cassava pulp Aspergillus oryzae Increased crude protein, true protein and decreased fibre contents [26]
Banana peel S. cerevisiae Increased the content of crude protein, crude fat, calcium and phosphorus and decreased crude fibre [27]
Banana peel Ch. Crassa and B. subtilis (two-stage fermentation) Increased crude protein and metabolizable energy, while decreasing crude fibre, fat and ash contents [9]
Wheat bran Bacillus cereus Increased crude protein and decreased crude fibre, natural detergent fibre and hemicellulose [28]
Wheat bran Mixture of Lactobacillus acidophilus, B. subtilis, S. cerevisiae and Lactobacillus rhamnosus Increased crude protein and acid soluble protein, while reducing starch, crude fat, crude fibre, neutral detergent fibre, acid detergent fibre and crude ash contents [19]
Maize bran Rumen filtrate Increased crude protein and metabolizable energy and decreased crude fibre contents [29]
Orange pulp S. cerevisiae Increased crude protein and decreased crude fibre contents [30]
Dried brewer’s grains S. cerevisiae, L. rhamnosus and B. Subtilis Increased crude protein and ether extract, and decreased crude fibre, neutral detergent fibre, acid detergent fibre and lignin [10]
Soybean hulls and Pleurotus eryngii stalk residue Aureobasidium pullulans Reduced non-starch polysaccharides content [6]

In feed industry, the agricultural byproducts may be fermented through submerged liquid fermentation or solid-state fermentation, depending on the natures of the substrates and the microbes used as fermentation starter [5, 20]. For the byproducts with high fibre contents, there has recently been a tendency to apply solid-state fermentation by using cellulolytic microbes [20]. In respect particularly to the microbes, Olukomaiya et al. [20] suggested that only a few microorganisms such as yeast and filamentous fungus, can thrive in solid-state fermentation conditions due to the low moisture requirements. Other than the natures of substrates and microbes, the quality of fermented products may be determined by the conditions during the fermentation process. Some adjustment and modifications may be conducted to optimize the fermentation process and the quality of fermented products. The addition of selenite to the substrate has been conducted by Sundu et al. [11] and ammonium sulphate by Hafsah et al. [12] when they fermented coconut dregs using Saccharomyces cerevisiae. When compared to fermentation without selenite or ammonium sulphate, they found that adding selenite or ammonium sulphate enhanced the content of crude protein and decreased crude fibre in the fermented products. It was most likely that selenite and ammonium sulphate could increase the population of the microbes and therefore increased the protein biomass and bioconversion of fibre into simple carbohydrate [11, 12]. Other method to optimize the fermentation process has also been conducted by Sugiharto et al. [8, 9] when fermented cassava pulp. They conducted two stages of fermentation using Chrysonilia crassa during the first fermentation stage and Bacillus subtilis for the second fermentation phase. When compared to the nutritional features of fermented items produced by a single fermentation process, the two-stage fermentation method produced greater nutritional properties.

4. Fermented agricultural byproducts as the alternatives to conventional protein- and energy-rich feed ingredients

The rise in prices as well as the negative environmental effects of soybean and maize cultivation has prompted poultry nutritionists to look for alternatives to conventional protein- and energy- rich feed ingredients for broilers. As a result, fermented feed based on agricultural byproducts appears to have a good chance of being included into broiler rations. A number of studies have been carried out to elucidate the possibility of using agricultural byproducts-based fermented feed in broiler rations. For example, Wang et al. [22] reported that using fermented cottonseed meal reduced the proportion of soybean meal in broiler chickens raised for 42 days by 10.14% (during the starter phase) and 7.5% (during the finisher phase) without adversely affecting growth performance, feed intake, and feed conversion ratio. According to Mirnawati et al. [31], palm kernel meal fermented with B. subtilis can replace up to 25% of soybean meal in broiler diets with negligible performance loss and a 50% cost reduction. Furthermore, Ahmad et al. [23] found that adding up to 15% fermented rice bran to broiler diets improved broiler performance. According to a previous study by Supriyati et al. [24], the use of Bacillus amyloliquefaciens-fermented rice bran for broiler chicks could account for up to 15% of the diet without causing harm. In the latter trial, fermented rice bran was found to lower the need of yellow maize as a source of energy for broilers. In line with this, Sundu et al. [32] used fermented palm kernel meal as the alternative energy source and hence reduced the proportion of yellow maize in broiler diets. They found that supplementation of the diets with 20% of palm kernel meal fermented with different fungi (Aspergillus niger, Pleorotus ostreatus and Trichoderma viride) could maintain body weight gain to the same level of those birds fed the basal diets. From day 12 to 35 days of rearing, Sugiharto et al. [7] included 16% Acremonium charticola-fermented cassava pulp in broiler diets. The use of such fermented cassava pulp lowered maize proportions by 13.5% and soybean meal proportions by 5.5%. They discovered that such inclusion had no negative impact on broiler final body weight, dry matter and organic matter digestibility, as well as nitrogen retention. Moreover, feeding fermented cassava pulp to broiler chicks lowered the feed cost per kilogram of live weight gain. In another study, Sugiharto et al. [8] reported that inclusion of the two-stage fermented cassava pulp to 20% at the expense of maize did not cause deleterious effect on the growth performance of broilers. Also, dietary inclusion of fermented banana peel meal at the levels of up to 15% had no detrimental effect on growth and health performances of broiler chickens [9]. Feng et al. [28] replaced corn (5%) in broiler diets with fermented wheat bran. They pointed out that the substitution had no negative effects on growth and instead increased digestive enzyme activity and the diversity of intestinal flora. In line with this, Zhang et al. [19] found that dietary addition of fermented wheat bran up to 300 g/kg to reduce the quantity of maize (26.74%) and soybean meal (13.23%) had no adverse effect on broiler growth performance. To lower the quantity of yellow maize in diets, Francisco et al. [29] also included maize bran for 22.5% during the finishing period of broiler rearing, and they reported no deleterious effect on growth performance of broilers. This feeding strategy also yielded better financial results (lower feed costs per bird and higher gross profit margins per bird). Recent study by Al-Khalaifah et al. [10] further showed that broiler chickens grew faster and had higher economic efficiency when their corn-soybean-based diet was replaced with 10% fermented dried brewer’s grains. In accordance with this, Teng et al. [33] previously documented that feeding wheat bran fermented with B. amyloliquefaciens and S. cerevisiae improved feed conversion ratio of broiler chickens. As a result of the increased feed efficiency, broiler producers were able to reduce their feed costs while increasing their profits.

Although the method of employing fermented agricultural byproducts in broiler feed can reduce feed costs and GHG emissions, it must be carefully considered and treated. Several factors must be addressed, including the fermented product’s quality (nutrient composition), its level in the ration, the components of other feed ingredients in the ration, whether or not a feed additive (e.g. enzymes) is required in the feed, and the broiler house conditions. With regard in particular to the levels of the fermented agricultural byproducts in broiler rations, formulating feeds is something to be concerned about. The nutritional values of the fermented agricultural byproducts and other feed ingredients must be considered so that broiler chickens’ nutritional requirements can be met even though they use feed ingredients at lower prices. One technique to increase the proportion or quantities of fermented agricultural byproducts in broiler diets is to use enzyme as a feed additive. This is motivated by the idea that enzymes help poultry digest their feeds better. Sugiharto et al. [34] used fermented papaya leaf and seed meal in the Indonesian crossbred chicken feeds in a recent study. They compared the chicks that were fed fermented feed to those that were fed fermented feed plus multienzyme. Multienzymes have been proven to improve feed conversion ratios and income over feed costs in the Indonesian crossbred chicken. The enzyme was most likely to improve digestibility and, as a result, feed utilization by the Indonesian crossbred chicken.

5. Feeding fermented agricultural byproducts to reduce carbon footprint

As discussed earlier, the use of fermented agricultural byproducts in broiler diets can reduce the need for yellow maize and soybean meal as the source of energy and protein, respectively. Considering that cultivation of corn and soybean is associated with the increase in carbon footprint, the use of fermented agricultural byproducts as the alternative to corn and soybean meal for broilers may therefore reduce the emission of GHG. Also the use of fermented agricultural byproducts as broiler feed can minimize the decomposition of agricultural byproducts that can produce GHGs [17]. It has widely been known that intensification of livestock production has led to increased atmospheric nitrogen loss due to manure production and management. In general, the content of organic matter in manure affects nitrogen emissions through mechanisms like composting, crust formation, mineralization-immobilization turnover, and water retention [35].

Nitrous oxide, which is one of the major GHGs, is an unwanted byproduct of nitric acid synthesis that results from the accidental oxidation of ammonia. According to Suffian et al. [14], the source of the biggest nitrous oxide emissions in modern broiler production is bedding. In this case, a higher ammonia content in the bedding materials may result in increased nitrous oxide emissions. The amount of ammonia in the bedding is generally linked to the amount of nitrogen excreted by the chickens. In this case, better protein digestibility may reduce nitrogen excretion, thus lowering ammonia levels in bedding materials. According to Lee et al. [6], feeding fermented agricultural byproducts enhanced feed digestibility while reduced nitrogen excretion. This suggests that feeding fermented agricultural byproducts increased the digestive enzyme activity, and hence promoted nutrient use by the chicks. In agreement with this, Alshelmani et al. [21] demonstrated that the nutrient digestibility has been increased significantly in broiler chickens fed palm kernel cake fermented with Paenibacillus polymyxya ATCC 842 or Weisella confusa SR-17b. Moreover, the digestibility of crude protein also increased with feeding palm kernel cake fermented using P. polymyxya ATCC 842 or W. confusa SR-17b. The improvement in feed digestibility of broilers fed fermented feed has actually been highlighted by Sugiharto and Ranjitkar [5]. They suggested that the presence of functional components, such as probiotics, and the less antinutrient substances in fermented feed may be attributed to the improved feed digestibility of broilers. In agreement with this, study in pigs by Ahmed et al. [36] confirmed that fermented feed reduces Escherichia coli levels in the intestine and improves crude protein digestibility, allowing for less substrate for microbial fermentation in the colon. This condition has an impact on ammonia emissions reduction. With regard particularly to the role of probiotics, Mahardhika et al. [37] reported that dietary administration of probiotics (mixture of Lactobacillus sp., and Bacillus sp., and Streptomyces sp.) increased feed digestibility and thereby reduced concentration of ammonia in the excreta of broilers.

In poultry, non-starch polysaccharides enhance digesta viscosity, and thus lowering feed digestibility in the small intestine [5]. Previously, Lee et al. [6] reported that fermentation reduced the content of non-starch polysaccharides in the agricultural byproducts. For this reason, feeding fermented agricultural byproducts may improve feed digestibility and eventually reduce ammonia emissions. Feeding fermented feed has been associated with the improved intestinal morphology of broilers, which is accounted to the improved digestive function and nutrient digestibility of chicks [5]. In line with this, Teng et al. [33] documented that feeding wheat bran fermented with B. amyloliquefaciens and S. cerevisiae increased villus height of intestine and thereby improved feed digestibility of broilers. In contrast to Lee et al. [6] who showed reduction of ammonia due to feeding fermented feed, Teng et al. [33] found no significant effect of feeding fermented agricultural byproducts on ammonia emissions in their study. Indeed, the efficacy of fermented agricultural byproducts in lowering ammonia emissions may be determined by the different capacity of fermented feed in modifying the balance of intestinal bacteria. According to Sugiharto and Ranjitkar [5], increased commensal bacteria (especially lactic acid bacteria) in the intestine may improve ecological (lower pH values) and morphological conditions (higher villi height to crypt depth ratio), resulting in increased feed utilization (especially protein) by the birds. Indeed, the increase in protein utilization may consequently decrease unutilized protein (uric acid and urea) that is eventually be excreted and converted to ammonia [38].

6. Mechanisms and functions of fermented agricultural byproducts in reducing carbon footprint

In addition to better nutritional quality, fermented products are typically characterized by a lower pH and a higher contents of lactic acid bacteria and organic acids [5]. Lower pH values in fermented agricultural byproducts have been associated with lower gut pH of broilers [5]. In this case, a lower pH can contribute to an improved microbial balance in the broiler gut. The latter condition consequently improves the morphology and thus the digestive and absorption functions of the broiler intestine [39]. Indeed, the improvement in nutrient digestibility, particularly protein digestibility, may consequently reduce nitrogen excretion as well as reduce the availability of substrates for caecal microbial fermentation and thereby lowering ammonia emissions [40]. It should be noted that microbial protein fermentation in caeca can result in the formation of ammonia [38]. The caecum is well known as the primary site of fermentation in chicken, and it is here that methanogenic bacteria employ byproducts of fermentation like H2 and CO2 to generate methane. Given that methanogenic bacteria thrive best in the pH range of 6.0–7.5, a drop in intestinal pH, particularly in the caeca, may therefore reduce the population of methanogenic bacteria and thus reduce methane production [41]. When considering the pH range for optimal methanogen growth in the caeca, increased ammonia production as a result of microbial protein fermentation may cause the pH of the caeca to rise. This environment may encourage the growth of methanogenic bacteria, resulting in higher methane emissions [38].

Organic acids have recently been used in broiler diets to improve the intestinal health and functions of broilers [42]. With regard particularly to fermented feeds, such products have been linked to a higher amount of organic acids, which are the end products of the fermentation process [5]. Study by Gao et al. [41] documented that feeding fermented rapeseed cake reduced methane and ammonia production in caeca of broilers. The latter authors further revealed that the increased numbers of total caecal bacteria (i.e., Lachnospiraceae, Lactobacillus spp., Streptococcus spp., Bacteroides spp., and Alphaproteobacteria) and reduced numbers of methanogen were attributed to the lower methane production in the caeca of broilers. With regard particularly to the lowering effect of organic acids-rich fermented products on ammonia production, recent study by Nguyen and Kim [40] reported that dietary administration of organic acids resulted in decreased excreta NH3 gas emission. The latter drop in NH3 gas emissions could be owing to a decrease in pathogenic bacteria in the gastrointestinal tract, or it could be due to a rise in beneficial microbial activity, which leads to changes in microbial fermentation end products. The capacity of organic acids in improving the feed digestibility may also be linked to the less GHGs emission, as confirmed by Nguyen and Kim [40]. In agreement with this, Yan et al. [43] revealed that faecal GHGs emission could be associated with feed digestibility, as higher feed digestibility may result in less substrate available for microbial fermentation in the caeca, thus lowering faecal GHGs gas emission.

The decrease in excreta NH3 emission of broilers has been attributed to the enhanced Lactobacillus population in the intestine [40]. As mentioned previously, the fermented agricultural byproducts contain a notable numbers of probiotic bacteria such as lactic acid bacteria. In this regard, feeding fermented agricultural byproducts is projected to increase the population of good bacteria in the intestine [5, 40], and hence improving the feed digestibility and lowering GHGs emission. In conjunction with this, Santoso et al. [44] documented that Bacillus subtilis-fermented product improved feed efficiency and utilization and thereby reducing the emission of ammonia from broilers. In this case, the presence of probiotic bacteria in fermented products was responsible for lowering the GHGs emission from broiler production. Indeed, Vimon et al. [45] reported that probiotic bacteria supplementation can increase feed digestibility through the improvement of intestinal ecology and functions as well as production of digestive enzymes resulting in minimum substrates for the microbial fermentation in the caeca of broilers. With regard particularly to caeca that is the primary fermentation site in poultry, feeding fermentation products has been reported to increase the population of lactobacilli in the caeca [46]. Considering the antagonistic activity of lactic acid bacteria against methane producer bacteria in the caeca [47], the increase lactobacilli with feeding fermented products may therefore reduce the numbers of methanogens and thus lowering methane production.

The role of fermented agricultural byproducts in lowering GHGs emission seems also to be associated with the positive impact of fermented products in increasing the activities of digestive enzyme in the gastrointestinal tract of poultry. Ashayerizadeh et al. [48] revealed that feeding fermented rapeseed meal increased protease and amylase activities as well as the digestibilities of energy, crude protein and crude fat. The latter conditions may therefore reduce caecal microbial fermentation and thus GHGs production. It has been observed that fermentation produces enzymes that are necessary for broiler digestion. In this respect, Hatta et al. [49] reported that fermentation of copra meal using a fungus Trichoderma viride produced cellulase that is crucial for fibre digestion in the small intestine of broilers. Indeed, the optimal fibre digestion in the upper part of the gastrointestinal tract may consequently reduce the available substrate for microbial fermentation in the caeca of broilers, thus lowering GHGs emission.

7. Conclusions and future perspectives

Despite the fact that broiler farming produces lower GHG emissions than other farms, feed production and broiler excreta are the primary sources of GHG emissions. Because maize and soybean meal are the two major ingredients for broilers, reducing the amount of these conventional feed materials in broiler diets by employing fermented agricultural byproducts could reduce maize and soybean cultivation, and hence the carbon footprint. Feeding fermented agricultural byproducts increased feed digestibility and nutrient utilization, lowering unutilized nutrients (particularly protein), and therefore lowering nitrous oxide emissions. The ability of fermented agricultural byproducts to improve intestinal conditions and functions in utilizing feed and nutrients may be used to measure the efficacy of fermented agricultural byproducts in minimizing GHG emissions from broiler production. On this basis, improving the quality and functional features (e.g., probiotic content) of the fermented agricultural byproducts may help to enhance feed digestibility and therefore reduce carbon footprint from broiler production. Further research is needed to quantify how much carbon dioxide equivalent could be reduced from broiler production by feeding fermented agricultural byproducts.

References
 
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