Carbohydrate Type and Level Affect in Vitro Methane Production from Cecal Contents of White Roman GeeseABSTRACT
The type of carbohydrate diet is an important factor in methane (CH4) emission from livestock. In this study, a structural carbohydrate (rice hull) was tested as a feed ingredient and compared with the use of a non-structural carbohydrate supplemented to cecal contents to study the effect of carbohydrates type and levels on methane production from the caecum content of White Roman geese. Four experiments were conducted to determine the methane production in the cecal material from White Roman geese. In Experiment I, the methane production in vitro from cecal content from the basal diet supplemented with 8% rice hull did not increase compared with the basal diet. In Experiment II, non-structural carbohydrates such as glucose, starch, and sucrose could increase the methane production of cecal contents in vitro (p<0.05), and the mean methane production was such that glucose > starch > sucrose. In Experiment III, the cumulative methane production in cecal contents added with glucose in White Roman geese for different incubation times showed that the methane production had the largest increase 0.5 hour after adding the glucose treatments. It also indicated that glucose could be fermented and converted into methane after half an hour of incubation. In Experiment IV, methane production from cecal contents increased with the quantity of glucose (p<0.001) in a dose response manner of additives, whereas methane concentration did not increase with the dose of glucose in geometric progression. These results suggest that rice hulls can substitute part of the feed of White Roman geese to reduce methane emissions. Methane production rates from cecal contents depend on the type of carbohydrate and the additional glucose in cecal can cause issues by increasing methane emission from birds. To conclude, it is suggested that the speed of decomposing polysaccharide into monosaccharide by digestion may be a key to determine methane production rate from cecal content in goslings.
Keywords:
Carbohydrate type; ceca; methane emission; geese
INTRODUCTION
Methane is one of the most important greenhouse gases, with 25 times more global warming potential than carbon dioxide according to the fourth report (AR4) of IPCC 2007 (Climate Change, 2007), even being set to a higher GWP of 28 according to AR6 in 2022 (Climate Change, 2022). Each year, livestock produces 80-115 million metric tons of methane, which amounts to 15% to 20% of the total emissions caused by humans (Climate Change, 2001). Methane production from enteric fermentation in ruminants is one of the major sources of anthropogenic greenhouse gas emission in the world (Boadi et al., 2004; Kebreab et al., 2008). In ruminants, the majority of enteric methane emission is from the rumen. Ruminant livestock can produce 250 to 500 liters of methane per day (Johnson et al., 2004). Enteric methane production arises mainly from microbial fermentation of hydrolyzed dietary carbohydrates (Crutzen et al., 1986; Solaiman et al., 2010). Many factors influence methane emissions from cattle, including the following: level of feed intake, type of carbohydrate in diet, feed processing, additional lipids or ionophores to the diet, and alterations in the ruminal microflora (Crutzen et al., 1986).
Geese are herbivorous animals that can digest dietary fiber. The digestibility of acid detergent fiber and neutral detergent fiber is 34.6% and 15.7%, respectively, for goslings feeds containing 8% crude fiber (Sue et al., 1996). Rice is the staple food crop in Taiwan, with an annual output of 1,700,229 tons, of which rice hull is a byproduct, with 332,014 tons per year production (Statistical Yearbook, 2020). In respect to rice hull, it is one of the common feed ingredients in commercial feed formulation for geese in Taiwan. Since geese are herbivores that can digest plant fiber, their enteric methane emissions are minimal and occur mainly from the ceca of the hindgut (Chen et al., 2014), with an enteric fermentation emission factor of 1.88 mg/bird/day for 9-week-old geese (Chen et al., 2003). It is unknown whether the cecum of geese has the same digestive function as the rumen in ruminants, or the CH4 concentration of cecal content in geese increases with increasing dietary fibers. Chen et al (Chen et al., 2021) reported that pH, incubation temperature, and nutritive solution are factors that influence cecum methane concentration in geese. Different carbohydrate types - i.e. glucose, monosaccharide - have been confirmed to be the major and direct source of methane production, as compared with disaccharides and polysaccharides (Solaiman et al., 2010). It is worthwhile to study in vitro CH4 production of cecal contents by feeding basal diets added with structural dietary fibers or adding nonstructural types of carbohydrates into cecal content. Therefore, the purpose of this study was to investigate the effect of carbohydrate types on levels of methane production in the caecum content of White Roman geese.
MATERIALS AND METHODS
Animal and Management
Four experiments were designed to examine the effect of carbohydrate type and levels on in vitro methane production from the cecal contents of White Roman geese. Measures were taken to ensure the homogeneity of management background. All animal subjects were selected as follows: In experiment I, twenty- four one-day-old robust and healthy White Roman goslings with similar body weight were selected from 32 goslings purchased from a commercial farm, and were used as experimental animals. The twenty-four goslings were divided into two treatments and allocated to three cages (90 cm × 56 cm × 60 cm) of 4 goslings each. The birds of two groups were fed basal diets based on NRC (NRC, 1994) recommendations (crude protein; CP: 20.4%; metabolizable energy; ME: 2943 kcal/kg, Table 1) and basal diet plus 8% crushed rice hull (CP:19.4%, metabolizable energy; ME: 2779 kcal/kg, Table 1), respectively. Feed and water were available ad libitum throughout the experiment (1-5 weeks of age). In Experiment II, III, and IV, geese were fed on a commercial diet (CP: 20.4%; ME: 2943 kcal/kg, Table 1), and the feed and water were also supplied ad libitum.
Sampling and Treatment
Experiment I: The objective of this experiment was to investigate the impact of high-level dietary fiber structure on gosling cecal matter methane production. At five weeks of age, six birds were randomly selected from each treatment group, fasted for five hours, and then allowed to resume feeding for another five hours. The fasting procedure followed that described by Lo et al. (2019) (Lo et al., 2019). Cecal contents were collected from each bird after sacrifice by jugular vein bleeding. From each bird, 1.25 g of cecal matter was loaded into a 15 mL tube containing a nutrient buffer (3.75 mL) (Salvador et al., 1993), with each sample run in four replicates. The tubes were flushed with 100% CO2, sealed by a butyl rubber stopper, shaken, and then anaerobically incubated at 38oC for 4h. This incubation period was chosen as methane production typically stabilizes by this time (Chen et al., 2021). At the end of incubation, 10% mercuric chloride (HgCl2) solution (0.2 mL) was added to each tube to halt bacterial activity, and a gas-tight syringe was used to collect the gas and transfer the methane to a methane level detector.
Experiment II: To investigate the effect of different non-structural carbohydrate sources on methane production in the cecal contents of 14-week-old geese, sixteen birds aged 14 weeks were randomly selected, sacrificed, and their cecal contents were collected. For each bird, 0.3 g of cecal content was placed in a 15 mL tube containing a nutrient buffer (3.75 mL). A total of 30 tubes were prepared and divided into five treatments: control (1 mL distilled water), glucose (1 mL of 0.5% glucose), sucrose (1 mL of 0.5% sucrose), starch (1 mL of 0.5% starch), and sodium carboxymethyl cellulose (CMC; 1 mL of 0.5% CMC). Each treatment was performed in triplicate. The vials were filled with 100% CO2, sealed with butyl rubber stoppers, and then anaerobically incubated at 38°C. Samples were shaken on a shaker for 0 and 4 hours. After each incubation period, bacterial activity was halted by adding 0.2 mL of 10% mercury chloride (HgCl2) solution. Methane concentration was then measured. Other experimental procedures followed the same protocol as Experiment I.
Experiment III: To examine the effect of glucose on the methane production rates of cecal contents of White Roman geese across various incubation times, sixteen geese, each 14 weeks old, were randomly selected, sacrificed, and their cecal contents collected. Each sample was pooled in a plastic beaker, and 0.3 g of cecal content was loaded into a 15 mL tube containing a nutrient buffer (3.75 mL). Thirty tubes were prepared and allocated to two treatments: a control group (with 1 mL of distilled water) and a glucose group (with 1 mL of 0.5% glucose solution). The tubes were flushed with CO2 (100%), sealed with a butyl rubber stopper, and anaerobically incubated for 0, 0.5, 1, 2, 3, and 4 hours at 38°C, with each treatment time conducted in triplicate. At the end of each incubation period, methane levels were measured with procedures consistent with those of Experiment I.
Experiment IV: To investigate the effects of different glucose concentrations on in vitro methane production of cecal contents of White Roman geese, sixteen 14-week-old geese were randomly selected, sacrificed, and their cecal contents sampled. Each sample was mixed in a plastic beaker, and 0.3 g of the cecal content was loaded into a 15 mL tube containing a nutrient buffer (3.75 mL). Thirty-six tubes in total were prepared and divided into three treatment groups: a control group (with 1 mL of distilled water), and two glucose treatments (with 1 mL of 1% and 2% glucose solution, respectively). The tubes were flushed with CO2 (100%), sealed with a butyl rubber stopper, and anaerobically incubated for 0 and 4 hours at 38°C, with each treatment conducted in triplicate. Following incubation, methane levels were measured with procedures consistent with those of Experiment I.
Methane concentration analysis was performed with a Shimadzu model 14 B gas chromatograph (Flame Ionization Detector) and a 2 m inner diameter Porapak Q column (Supelco, PA, USA). The oven, injection port, and detector were all maintained at 70°C and 130°C, respectively. Nitrogen (98.5%) was used as the carrier gas at a 10 mL/min flow rate, and methane gas (95.5%, China Petroleum Co.) diluted with nitrogen to concentrations of 10, 50, 100, 500, and 1000 ppm was used as reference to construct a standard curve. Methane levels were calculated as described by Wang et al. (Wang et al., 2003). The standard curve for CH4 demonstrated linearity, with a minimum detection concentration of 0.5 ppm, an R²>0.998, and a Coefficient of Variation (CV) < 4.7%. The reference standard of 100 ppm was retained as an inter-assay quality control (QC), achieving a CV below 10% for consistent accuracy.
Statistical Analysis
Both qualitative and quantitative data analyses were performed by Analysis of Variance using the general linear model procedure. All statistical analysis was carried out using SAS software (SAS, 2014). The least square means were used to compare and estimate the differences between or among the treatments in each experiment.
RESULTS
Methane Generation of the Cecal Contents at High and Low Dietary Fiber Levels
The goslings had a higher relative cecum length when receiving feed with 8% rice hull treatment than that of the control treatment (p<0.05; Table 2). However, there were no significant differences in feed intake, relative cecum content weight, or methane production.
Methane Generation of the Cecal Contents Adding Different Types of Carbohydrates
Table 3 shows the methane production in the cecal contents with different types of carbohydrates. Among the treatments, cecal contents supplemented with glucose showed the highest methane concentration. Adding any carbohydrate type, except for CMC, significantly increased methane production (p<0.05). The order of methane concentration from highest to lowest was: glucose > starch > sucrose > CMC > control. Furthermore, compared with the control, the cumulative methane production of cecal contents after 4 hours of incubation with 0.5% levels of CMC, starch, sucrose, and glucose increased by 1.76, 10.8, 7.3, and 14.4 times, respectively.
The Cumulative Methane Generation in Cecal Contents by Adding Glucose
Table 4 displays the cumulative methane production from the cecal contents, with and without added glucose, across different incubation times. The results indicate that the methane production rate increased most sharply at 2-3 hours in the control group, and at 0-0.5 hours in the glucose treatment group. During these periods, methane production in the cecal contents increased by 50.3 times in the control group and by 28.4 times in the glucose treatment group, compared to the initial levels at the start of incubation. At each incubation time, except for 0 and 0.5 hours, the cumulative methane production was significantly lower in the control group compared to the glucose-added group (p<0.05). Additionally, methane concentrations in the cecal contents increased linearly with incubation time in both the control and 0.5% glucose treatments (p<0.001). The regression equations for methane production (M, in μg/g) as a function of incubation time (T, in hours) were as follows: for the control group, M=−13.25+39.31T (R²=0.89, p<0.001); and for the 0.5% glucose treatment group, M=−7.37+143.98T (R²=0.97, p<0.001).
The Effect of Glucose on the In Vitro Methane Production Rate
Table 5 illustrates the impact of glucose levels on methane production. A significant difference in methane production among the three treatments was observed (p<0.05). The cumulative methane production from cecal contents supplemented with 0%, 1%, and 2% glucose increased in the following order after 4 hours of incubation: 40.2, 143.5, and 253.5 times, respectively, compared to the initial incubation levels. Methane concentrations of cecal content increased linearly with increasing level of glucose (p<0.001). The relationship between level of glucose and methane production was shown by linear function as follows: M=278.0+608.79L (R2=0.96; M: methane production, ug/g/4h; L: % glucose).
DISCUSSION
Methane Generation of the Cecal Contents at High and Low Dietary Fiber Levels
Basal diet and the metabolized energy of the diets was decreased by adding 8% rice hull. Nevertheless, the feed intake of the geese did not increase during the whole experimental period. This phenomenon may result from the bulkiness of rice hull and the increase in the volume of the diet. Therefore, the feed intakes of birds were restricted because of the limited volume of the intestine. There was a higher relative cecum length of birds in the treatment receiving feed supplementation with 8% rice hull. This result is consistent with that reported by Abdelsamie et al. (Abdelsamie et al., 1983), which showed that the relative length of ceca in broiler increased with dietary acid detergent fiber contents. Dietary fiber levels effectively elongated the relative length of the ceci of geese. Methane production of cecal content in gosling did not increase with increasing dietary fiber, a result that does not coincide with the report of Aguerre et al. (Aguerre et al., 2011), who showed that increasing the forage-to-concentration ratio from 47: 53 to 68: 32 increased CH4 emission. However, the result of Experiment I is consistent with Tsukahara et al. (2000), who indicated that chicken feed with soybean meal containing 7.7% crude fiber level and the amount of methane produced from cecal content of birds were less than that of meat meal containing 0.7% crude fiber, which indicated that dietary protein may play an important part in methane production for chicken. Clauss et al. (2020) suggested that dietary protein affects the methane emissions of geese. The report of Crutzen et al. (1986) noted that the methane release rates from ruminants were higher when fed with crude fiber. The reasons for the methane production of cecal content in basal diet supplemented with 8% rice hull not increasing compared with the basal diet treatment are the following:
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Structure fiber did not ferment easily into short-chain fatty acid. Reinhart et al. (1996) and Chen et al. (2009) point out that formic acid is a methane precursor, suggesting that formic acid concentration may be low in ceca of geese.
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The protein composition of diet changed: dietary conditions affects the hindgut fermentation through the selection of a particular microflora (Tsukahara et al., 2000). Fahey et al. (1988) pointed out that methanogenic bacterium may be affected by changes in diet. Tsukahara et al. (2000) suggested that dietary protein level is one of the important factors affecting the amount of methane production in cecal contents.
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A short retention time of digesta in bird ceci: Digesta retention time is less than 24 hours because the cecal contents of goslings are emptied once every 4 hors (Yang et al.,1975), once a day in turkeys (Duke et al.,1984), and once every 8.5 hors in ptarmigan (Gasaway et al.,1975); however, the mean retention time in the reticulo-rumen of 1 mm long particles with a density of approximately 1.0 g/ml is about 67h (Kaske et al.,1990). Therefore, the time of fermentation of cell wall carbohydrates is insufficient to produce methane in the ceca of goslings, and the methane production does not increase in the same pattern as ruminants.
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Different microbial colonies: Ciliates abound in the rumen, but apparently no protozoa live in the avian caecum, except as pathogens (G. Monachon, pers. com.) (Mattocks et al., 1971), which is also observed in turkeys (Bedbury et al., 1983). However, ruminal protozoa can reach numbers as high as105-106 cells/mL, and some protozoa digest cellulose and up to one-third of fiber (Czerkawski et al., 1986; Ogimoto et al., 1981; Russell et al., 2001). Methanogens living on and within rumen ciliate protozoa may be responsible for up to 37% of the rumen methane emissions, and in the absence of protozoa, rumen methane emissions are reduced by an average of 13%, although this varies with diets (Hegarty et al.,1999).
Methane Generation of the Cecal Contents when Adding Different Type Carbohydrates
The study of Wang et al. (Wang et al., 2004) indicated that higher CH4 production was found with a diet containing soluble dietary fiber compared with a low-soluble fiber diet in pigs. Structural carbohydrates originating from the cell wall of a plant may not have been easy to decompose by enteric bacteria in experiment I. Therefore, a series of non-structural carbohydrates were added to the cecal contents of birds in Experiment II. To summarize, the result demonstrates that soluble carbohydrates can stimulate methanogensis, with glucose causing the highest increase in the quantity of methane production among the four types of carbohydrates. Consequently, glucose is the major source for methane production in the cecum, a finding that agrees with the results of Williams et al. (1984), which showed that soluble carbohydrates (e.g., glucose) increase methane production.
The reason why the mean methane concentration from cecal contents added with different carbohydrates are in order of glucose > starch > sucrose > CMC > control may be related to hydrogen production, since H2 and CO2 are produced as glucose is converted into acetate or butyrate (Fang et al., 2002). Kumar et al., (2000) showed that the maximum rate of hydrogen production followed the order sucrose > CMC, while Solaiman et al. (2010) indicated that carbon dioxide combines with hydrogen to produce methane. Therefore, it may be supposed that the hydrogen yields follow the order glucose > starch > sucrose > CMC > control at the fermentation period.
The Cumulative Methane Generation in Cecal Contents by Adding Glucose
In Experiment II, it was confirmed that glucose is a major carbon source of methane in the cecal content of geese. Therefore, it is necessary to know when methanogensis came from glucose. In Experiment III, the methane production rate was beginning to increase at 0-0.5 hours of incubation; however, it was the highest at 2-3 hours for the glucose-treated group. This indicates that glucose is fermented fast by enteric bacteria of the ceca during the first half hour of incubation. Adding glucose into cecal contents increases methane production rates by increasing hydrogen supply (Fang et al., 2002), and it may be beneficial for hydrogen to combine with dioxide carbon into methane, or glucose is converted into formate, the precursor of methane (Solaiman et al., 2010). The phenomenon is similar to that observed in Experiment II.
The Effect of Glucose on the Methane Production Rate In Vitro
The study on the relationship between the dose of glucose and methane concentration found that the latter did not increase in proportion to the increase in the dose of glucose, but increased 3.66 and 1.58 times while the glucose dose increased from 1 to 2 times, respectively. Methane production seems to be suppressed by acetic acid during the fermentation process, as glucose could be converted into acetic acid (Fang et al., 2002), and the pH of cecal contents may drop as an amount of acetic acid is produced, which is unfavorable to methanogenesis. Van Kessell et al. (1996) showed that methane production plummeted at pH values below 6.5, and virtually no methane was produced at a pH lower than 6.0. Other studies also showed that acetic acid inhibited methane generation (Chen et al., 2009; Van Kessell et al., 1996). Therefore, acetic acid and pH may inhibit methane generation rates in the cecal contents when the glucose dose is above 2%.
CONCLUSION
This study suggests that increasing dietary fiber from rice hulls does not raise methane production in gosling cecal content in vitro. This implies that using rice hulls in feed could be beneficial for reducing greenhouse gas emissions in waterfowl. Additionally, glucose significantly increases methane production in White Roman goslings’ cecal contents, particularly after 4 hours of incubation, indicating its role as a major methane source. Methane production peaks at different times for glucose and control groups, emphasizing the rapid conversion of glucose to methane by cecal bacteria. Furthermore, while insoluble polysaccharides from rice hull fiber do not increase methane production, soluble monosaccharides and glucose do, suggesting that methane emissions in geese may not only depend on dietary protein but also on the type of digestible carbohydrates.
ACKNOWLEDGEMENTS
The authors are greatly appreciative of the Green Energy Development and Management Institute (TGEI) in Tunghai University for their financial support and a part of NSTC113- 2622-8-143-001-TH.
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FUNDING
This study was financially supported by the Tunghai Green Energy Development and Management Institute of Tunghai University.
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DATA AVAILABILITY STATEMENT
Data will be made available on request.
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DISCLAIMER/PUBLISHER’S NOTE
The published papers’ statements, opinions, and data are those of the individual author(s) and contributor(s). The editor(s) disclaim responsibility for any injury to people or property resulting from any ideas, methods, instructions, or products referred to in the content.
Data will be made available on request.
