Research Article

 

Effect of Dietary Supplementation Based on Ammoniated Palm Frond with Saccharomyces cerevisiae and Gambier Leaves Waste on Nutrient Intake and Digestibility, Daily Gain and Methane Production of Simmental Cattle

 

Rusmana Wijaya Setia Ningrat1*, Mardiati Zain1, Elihasridas1, Malik Makmur2, Ezi Masdia Putri2, Yesi Chwenta Sari1

1Department of Animal Nutrition and Feed Technology, Faculty of Animal Science, Andalas University Kampus Limau Manis, Padang - 25163, Indonesia; 2Graduate School of Animal Nutrition and Feed Technology, Faculty of Animal Science, Andalas University Kampus Limau Manis, Padang - 25163, Indonesia.

 

Received | June 13, 2020; Accepted | August 15, 2020; Published | November 15, 2020

*Correspondence | Rusmana Wijaya Setia Nngrat, Department of Animal Nutrition and Feed Technology, Faculty of Animal Science, Andalas University Kampus Limau Manis, Padang - 25163, Indonesia; Email: [email protected]

Citation | Ningrat RWS, Zain M, Elihasridas, Makmur M, Putri EM, Sari YC (2020). Effect of dietary supplementation based on ammoniated palm frond with saccharomyces cerevisiae and gambier leaves waste on nutrient intake and digestibility, daily gain and methane production of simmental cattle. Adv. Anim. Vet. Sci. 8(12): 1325-1332.

DOI | http://dx.doi.org/10.17582/journal.aavs/2020/8.12.1325.1332

ISSN (Online) | 2307-8316; ISSN (Print) | 2309-3331

Copyright © 2020 Ningrat et al. This is an open access article distributed under the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited.

 

INTRODUCTION

 

Palm frond (Elaeis guineensis) is agriculture by product that potential to be used as fiber feed for ruminants (Zain et al., 2008; Suryani et al., 2017). Optimizing the utilization of palm frond need to be followed to attempt to maximize rumen microbial growth with additional treatment. One approach that can be used is the addition of microbial supplements (Zain et al., 2011, Herawaty et al., 2013). Saccharomyces cerevisiae (SC) is one of the fungal direct-fed microbes that can increase fiber degradation by providing an optimal rumen environment through oxygen reduction and lactic acid accumulation and stimulating the growth of endogenous fungal rumen. (Suryani et al., 2015). It was reported that the supplementation of fungal culture was able to increase total VFA and the digestibility of fiber fractions in hay or forage basal diets (Plata et al., 1994). Therefore, supplementation of S. cerevisiae can to increase performance of ruminants.

 

The utilization of palm frond oil as a basal diet of is constrained by high lignocellulose content in plant vegetative tissue. High fiber fraction affects a longer rate of passage rumen and does not fulfill daily metabolic energy requirements for ruminants (Ginting et al., 2018). Ammoniation and probiotic fungal supplementation provide favorable results on agricultural waste (Zahari et al., 2003; Zain et al., 2011; Chanjula et al., 2018). High fiber content on tropical feedstuff not only lowers feed efficiency but also increases the production of enteric methane (CH4) in the ruminant. Several studies providing a variety of diets from natural tannins including gambier leaves on in vitro, in sacco, and in vivo evaluation have had a positive influence on performance and quality of ruminant products (Alam et al., 2007; Garcia et al., 2019; Natalello et al., 2019). The combination of these methods is expected to provide optimum animal performance.

 

Potential sources of natural tannins that are abundantly available in the West Sumatra region are those derived from squeezed residues from gambier leaves (Uncaria gambir Roxb.) or called Gambier Leaves Waste (GLW). Polyphenol fractions detected in gambier leaves were mostly catechin acid (40-61%), tannin (16-25%), and a small portion of pyrocatechol, gambirin and quercetin (Yeni et al., 2014; Nurdin et al., 2018). In vitro studies show that supplementation of 15% GLW (as a source of tannin) with basal feed in the form of ammoniated oil palm frond can reduce the production of methane gas up to 53% and increase the digestibility of feed nutrients (Ningrat et al., 2017). Tannins have the capability as an anti-methanogenic agent on rumen methanogenic microbes (Makkar et al., 2007).

 

This shows satisfactory results at the in vitro level of SC and GLR which can stabilize rumen fermentation process while reducing the production of methane gas. However, the impact of synergy between the use of probiotics and botanical extracts simultaneously on increasing fiber digestibility, nutrient utilization, and ruminant growth performance still requires further study at an in vivo level (Arowolo et al., 2018). We hypotized that supplementation combination of S. cerevisiae and gambier leaves waste could increase Simmental cattle performance as well as decrease methane gas production.

 

MATERIALS AND METHODS

 

The oil palm fronds that have been chopped are prepared for the ammoniation process using urea at a level of 4% and chicken manure at 15% from dry matter content of oil palm fronds. After chicken manure is stirred evenly on substrate. Then urea is dissolved in water (1:1) and sprayed thoroughly on palm fronds. The ammonia process takes place under anaerobic conditions using a plastic container for 1 week. after the ammonia process is complete, the plastic seal is opened and palm fronds are dried to remove odor. Palm fronds are ready for consumption by livestock and further nutritional analysis. Pure yeast culture of S. cerevisiae (4 × 108 live organisms/g) was obtained from the Biotechnology Laboratory of Gajah Mada University, Yogyakarta Indonesia collection, strain Meyen ex Hansen). The methods of preparation for the growth medium of S. cerevisiae following procedure Zain et al. (2016). The addition of probiotic S. cerevisiae to an experimental diet was given at a level of 1% of the DM ration. GLW is obtained from gambier plantations in Painan and Payakumbuh in the province of West Sumatera. Gambier residue is a by-product of gambier extraction (leaves and stems) through conventional methods that consisted of boiling for 1.5 hours and squeezing plant materials (Anggraini et al., 2011).

 

The animal trial was arranged with four male Simmental cattle with 175-200 kg BW equipped were randomly distributed in a 4 x 4 Latin square design. The treatments were (A) 40% APF + 60% concentrate + mineral S and P (B) A + SC (C) A + GLW and (D) A + SC + GLW. The basal diet contained (dry basis) 40% ammoniated palm frond and 60% concentrate. The Composition and nutrient contents of feeds including concentrate are shown in Table 1.

 

Digestibility trials conducted using four animals for each treatment which were separated in individual pens. Cattles were fed ad libitum during the adaptation period (15 days) and then restricted during the collection period (6 days) at 90% of the intake feed that was offered at 7:00 and 16:00 h. In the last 15 days of each preliminary periods, animals were equipped with bags fitted to the animals with harness for total collection. Live weight gain was measured every two weeks. During the collection period, accurate records were kept for individual feed intake. Feed intake measured using the difference between the weight of given feed (kg) and the weight of remaining feed (kg) for one day. Determination of feed intake for nutritional attributes of DM, OM, and CP follows the formula: Feed consumption (kg.day-1) ×% DM × % nutritional attributes.

 

Total fecal excretion was collected once daily and 10% representative samples were dried at 60°C overnight and kept in sealed bags until further analysis. Feed and fecal were ground to pass through a 1-mm screen and composite. Dry matter, organic matter and nitrogen were analyzed by standard methods (AOAC, 1990). Neutral Detergent Fiber (NDF), Acids Detergent Fiber (ADF), cellulose were determined by the procedures outlined by Goering and Van Soest (1970). Digestibility of nutritional items are determined by reducing the amount of feed nutrients consumed (kg/head/day) and contained in feces by the following formula:

 

Digestibility = [(Feed nutrition consumption - feces) / nutrient consumption of feed] × 100%.

 

Table 1: Composition and nutritional content of experimental diet (% DM)

Items	Diet (% DM)
	A	B	C	D
Ammoniated palm frond	40	40	40	40
Rice bran	15	15	15	15
Palm Kernel Cake	33	33	33	33
Corn	10	10	10	10
Mineral	1	1	1	1
Salt	0.5	0.5	0.5	0.5
Sulphur (S)	0.3	0.3	0.3	0.3
Phosphorus (P)	0.2	0.2	0.2	0.2
Total	100	100	100	100
Suplementation
S. cerevisiae (SC)	-	1	-	1
Gambier leaf waste (GLW)	-	-	15	15
Nutrient Contents
Crude Protein	12.98	12.98	12.72	12.72
Fat	4.25	4.25	3.99	3.99
TDN	63.28	63.28	62.30	62.30
NDF	56.04	56.04	55.86	55.86
ADF	42.03	42.03	42.18	42.18

 

The accumulated urine was stored in a glass container with mixture of 10% H2SO4 for further allantoin analysis. The resulting methane was measured using Jentsch’s equation (Jentsch et al., 2007).

 

Methane production (MJ/day) = 1.62 dCP-0.38 dCfat+3.78 dCF+149 dNFE+1142 kg/day

 

Where:

dCP = Digestible crude protein

dCfat = Digestible crude fat

dCF = Digestible crude fiber

dNFE = Digestible nitrogen free extract

 

Statisical Analysis

Analysis of variance (ANOVA) was performed to test for correlations between the data parameters. Any correlations were tested further for statistical significance using the Tukey test (Steel and Torrie, 1980).

 

RESULTS AND DISCUSSION

 

Effect of Treatments on Nutrient Digestibility

Data of digestibility nutrient could be seen in Table 2. Supplementation of single S. cerevisiae could increase digestibility of DM, OM, NDF, ADF and cellulose, but supplementation combination of SC + GLW significantly increase (P<0.05) digestibility of nutrient. Studies conducted by Rivera-Mendez et al. (2017) showed that condensed, hydrolyzable, and tannin combination in Holstein steers gave an increase in dry matter intake by 4% -7.1%. The supplementation of S. cerevisiae in diet was able to stimulate the growth of microbes in the rumen and improve the digestibility of feed on ruminants (Zain, et al., 2011). Supplementation of SC could stimulate cellulolytic bacteria growth, can also inhibit the work of pathogenic bacteria (Denev et al., 2007). Reduced activity of pathogenic bacteria such as protozoa in rumen will stimulating population of beneficial rumen microbes. Increasing the population of rumen microbes, it can increase the activity of degrading the organic matter, thereby increasing the absorption of organic substances. This is supported by Kamel et al. (2004), which states that there is an increase OM digestibility with the supplementation of SC compared to the control.

 

Supplementation of SC + GLW more improves nutrient digestibility over the treatments. Besides the SC role, this is related to tannin content in the gambier leaves waste which has a positive effect on increasing efficiency of nutrition absorption in animal. Prasetiyono et al. (2018) reported that the addition of tannins from gambier to protect soybean meal protein resulted DM, OM, and rumen undegradable protein of 86.20%, 84.40%, 69.20%, respectively. Tannins produce favorable conditions for rumen microflora and suppress protozoa populations (Goel et al., 2008). The increased population of bacteria results in producing higher activity of extracellular enzymes that contribute to the digestion of nutrient compounds in feed. This is in agreement with our previous study (Ningrat et al., 2017; Ningrat et al., 2019) which found tannins func

 

Table 2: Digestibility nutrient of Simmental cattle with experimental diet

 

Nutrient digestibility (%)	Treatment				S.E.
	A	B	C	D
Dry matter	57,75c	61,55b	62,82b	65,07a	0.41
Organic matter	61.78c	65.45b	67.52b	71.52a	0.30
Crude protein	72.50	75.16	75.41	77.41	0.47
Acid detergent fiber	46.10c	52.14b	51.40b	55.40a	0.65
Neutral detergent fiber	48.06b	55.31a	54.18a	55.18a	0.68
Cellulose	47.83b	54.25a	53.18a	56.18a	0.76

Description: Different letters (a,b,c) in the same rows indicate significant differences (P<0.05); S.E.: standard error

 

tioned as defaunation agents capable of supressing the protozoa population up to 60%-70%. McLeod (1974) states that tannin molecules can disrupt the integrity of the cell wall and membrane of the protozoa, hence destroying the structure of the protozoa. Doležal et al. (2005) reported that the supplementation of SC to dairy cows at a dose of 10 grams/cow/day gave a trend of increasing protozoa populations 27% higher than control treatments. In vivo studies on buffalo bulls show a significantly increased effect of SC supplementation on protozoa populations and total bacterial rumen (Kumar et al., 2013). In high-fiber feed, protozoa prey on rumen bacteria reducing their number and level of fiber degradation. By reducing protozoa population, the bacteria population increases as indicated by the higher accumulation of allantoin levels in the urine of animals fed gambier leaves waste.

 

SC could modify the rumen ecosystem would be better to degrade fiber (Suryani et al., 2016). The study conducted by Zhu et al. (2017) showed that SC fermentation products in the range of 60-180 g/d with a low-quality forage diet could increase population of several species of ruminal cellulolytic bacteria, namely Ruminococcus albus, R. flavefaciens, and Fibrobacter succinogenes and a number of lactic acid bacteria (Selenomonas ruminantium and Megasphaera elsdenii). This further emphasizes the benefits of SC inclusion in low-quality forage rations to promote better digestion efficiency.

 

Supplementation of SC + GLW significantly (P<0.05) could increase fiber digestibility. There are strong evidence of synergic effect between yeast culture and plant extract to improve animal production. S. cerevisiae supplementation could improve digestibility of NDF, ADF and cellulose. This is in accordance with the results of research Whitley et al. (2009) suggest that there is an increase in NDF and ADF compared with controls. This is supported by Kamel et al. (2004) and Zain et al., 2011 stated that ADF digestibility increases with the addition of SC better than controls. The effect of supplementation yeast culture to ADF digestibility was also described by Chaucheyras-Durand et al. (2012), which states that yeast culture (SC) can stimulate the growth of rumen bacteria, especially cellulolytic bacteria and lactic acid bacteria. This is indicate that supplementation GLW could increase digestibility of NDF and ADF. Supplementation GLW increased digestibility of NDF and ADF at a level 15% of DM. This was due to the role of tannin in degradation of nutrient. Supplementation of GLW 25% tend to decrease digestibility of NDF and ADF. Increasing doses of tannin more than 15% reduced NDF and ADF digestibility (Ningrat et al., 2017). The low ADF digestibility due to high amounts of tannin could inhibit bacterial digestion and decrease performance of animals, especially in feed intake and nutrient digestibility (Smith et al., 2005).

 

Effect of Treatments on Cattle Performance

Data of DMI, OMI, ADG, methane production and allantoin urine of the experimmental rations with and without SC and GLW supplements are summarized in Table 3. Supplementation of SC and GLW had no significantly different (P>0.05) on DMI, OMI, and urine allanttoin. Combination of SC + GLW significantly (P<0.05) increase ADG and decrease methane gas production compared to control and treatment B, C. The highest mean value of ADG is treatment D (1.22 kg day1) and the lowest value is treatment A (0.75 kg day1). Supplementation of S. cerevisiae on diet were able to produce microorganism balance that beneficial on nutrient degradation in rumen (Williams and Newbold, 1990). Previous studies showed supplementation of SC on cattle diet could improved rumen fermentation characteristics, organic matter and protein digestibility as well as live weight gain in ruminant (Zain et al., 2011; Herawaty et al., 2013; Kamal et al., 2013) According to (Makkar, 2003) a decrease in animal’s feed intake has been observed only when the inclusion of tannin in diets is greater than 3% of DM. In this study, supplementation of S. cerevisiae and GLW as tannins source influencing on DMI, OMI and protein intake. These results are in accordance Alves et al. (2011) found no effect of tannins supplementation in the diets on DM intake.

 

Although there was no significant difference between treatments on nutrient intake the table showed that nutri

 

Table 3: Feed intake, average daily gain, methane gas production and allantoin urine of Simmental cattle with experimental diet.

 

Items	Treatment				S.E.
	A	B	C	D
Dry matter intake (kg.day-1)	5.75a	5.96a	5.87a	5.55a	0.06
Organic matter intake (kg.day-1)	5.13a	5.35a	5.67a	5.06a	0.05
Crude protein intake (kg.day-1)	0.67a	0.70a	0.72a	0.74a	0.01
Urine allantoin (L/d)	195.03a	225.68a	202.25a	206.40a	27.52
Average daily gain (kg)	0.75c	0.90b	0.92b	1.22a	0.02
Methane gas production (MJ.day-1)	2.36a	1.42b	1.35b	1.02c	0.05

Description: Different letters (a,b,c) in the same rows indicate significant differences (P<0.05); S.E.: standard error

 

ent intake were best result in treatment D. This indicated that supplementation of SC + GLW in complete feed of ammoniated palm frond could improve the digestibility of the treatment ration. This is presumably because SC can better modify rumen ecosystems for the development of rumen microbes in fiber digesting (Zain et al., 2011). SC was reported as a potential probiotic for ruminants through improved rumen fermentability by increasing total volatile fatty acids, iso-valerate acid, and reduction of acetate: propionate ratio (Riyanti et al., 2016).

 

Supplementation of SC + GLW on urine alantoin level could be seen in Table 3. Urine alantoin level can describe microbial protein synthesis. The higher content of urine alantoin microbial protein synthesis is increasing. SC + GLW supplementation was significant different (P <0.05) to increase urinary alantoin levels compared with controls. There were no significant differences between treatments B, C and D. These results are in accordance with studies conducted by Zhao et al. (2019) which combines tannins and cellulases in sheep thus providing a significant increase in nutrient digestibility, liver protein synthesis, and growth performance.

 

The increase in ADG is shown in Table 3 which indicates there is a statistically significant higher ADG in cattle feed the SC + GLW compared to other treatment. This is further evidence of an increase in feed digestibility possibly because the influence of feed with tannin content reduces rumen methanogenesis activity. Carulla et al. (2005) and Tan et al. (2011) state that natural tannins from tropical legumes produce more available nutrient content for animal production. Another hypothesis indicated that tannins from GLW produce less rumen degradable protein and more rumen undegradable protein and resulted in higher flows of essential amino acids available for absorption into the lower digestive system (Barry and McNabb, 1999; Min et al., 2003). Increase of ADG by S. cerevisiae, caused a DM intake, protein increased, also higher nitrogen retention (Hau et al., 2004). Saccharomyces sp. could stimulate growth of rumen bacteria especially cellulolytic bacteria which influence feed intake and digestibility of as influence the ADG (Callaway and Martin, 1997). There is a synergic effect when S. cerevisiae combine with tannins.

 

Effect of SC + GLW on methane gas production could be seen in Table 3. Supplementation of SC + GLW was significantly (P<0.05) could decrease methane gas 57% production compared to control. This is because tannins might be suppressing population of protozoa in rumen ecology (Patra and Saxena, 2010). The previous of in vitro studies showed that 0.4% tannin extracts from gambier leaves can protect extruded soy flour from rumen degradation, reduce methane gas production up to 25% and total gas production by 19% (Sajati et al., 2012). In vivo evaluation on Bos taurus × Bos indicus crossbreed shows the effect of 80% of Leucaena sp. (21% condensed tannins) in ration composition was able to reduce methane emissions by 61.3% without affecting dry matter intake, organic matter intake, and VFA production (Piñeiro-Vázquez et al., 2018).

 

The mechanism of inhibition of methane production in ruminants by tannin compounds has been initiated (Tavendale et al., 2005) i.e. (1) indirectly via inhibition of fiber digestion which reduces the production of H2, and (2) directly inhibits the growth and activity of methanogens. This indicates that the tannin content in the GLW is affecting the ruminal methanogenesis pathway by suppressing protozoa numbers (Goel et al., 2008) and has had a toxic effect on methanogenic bacteria (Carulla et al., 2005). At lower doses (5% of DM), reported tannin extracts from gambier leaves were reported not to show significant anti-methanogenic activity besides only affecting ammonia formation in vitro (Sinz et al., 2019). Besides that, SC had potential to reduce methane production, SC was able stimulate acetogens to compete with methanogen bacteria (Chaucheyras-Durand et al., 1995).

 

CONCLUSION

 

The combination supplementation of 1% S.cerevisiae and 15% gambier leaves waste in ration based on ammoniated oil palm frond was able to improve the nutrient digestibility, daily gain, and decrease methane production of Simmental cattle.

 

ACKNOWLEDGMENTS

 

This study was supported by INSINAS research by Ristekdikti contract No.SP2HL/LT/DRPM/III/2017. The research would not have been possible without the cooperation of my graduated student and technical assistance of Ruminant Nutrition Laboratory, Faculty of Animal Science, Andalas University.

 

CONFLICT OF INTEReST

 

All authors declare that there is no conflict of interest

 

authors contribution

 

Rusmana Wijaya Setia Ningrat, Mardiati Zain, and Elihasridas formulated the exper­imental design and did experimental work. Malik Makmur, Ezi Masdia Putri, and Yesi Chwenta Sari analyzing the data and drafted manuscript. All the authors read and approved the final version of the manuscript.

 

REFERENCES

 

• Alam M, Amin M, Kabir A, Moniruzzaman M, McNeill D (2007). Effect of tannins in Acacia nilotica, Albizia procera and Sesbania acculeata foliage determined in vitro, in sacco, and in vivo. Asian-Australas J. Anim. Sci. 20:220-228. https://doi.org/10.5713/ajas.2007.220

• Alves AR, Beelen PMG, De Medeiros AN, Neto SG, Beelen RN (2011). Consumo e digestibilidade do feno de sabiá por caprinos e ovi-nos suplementados com polietilenoglicol. Revista Caatinga. 24: 152-157.

• Anggraini, T, Tai A, Yoshino T, Itani T. (2011). Antioxidative activity and catechin content of four kinds of Uncaria gambir extract from West Sumatra, Indonesia. Afr. J. Biochem. Res., 5: 33-38.

• AOAC (Association of Official Analytical Chemists) (1990). Official Methods of Analysis of the AOAC. AOAC Inc. Arlington.VA. USA.

• Arowolo MA, He J (2018). Use of probiotics and botanical extracts to improve ruminant production in the tropics: A review. Animal Nutrition. 4: 241-249. https://doi.org/10.1016/j.aninu.2018.04.010

• Barry TN, McNabb WC (1999). The implications of condensed tannins on the nutritive value of temperate forages fed to ruminants. Br. Jr. Nutr. 81: 263-272. https://doi.org/10.1017/S0007114599000501

• Carrula JE, Kreuzer M, Machmiller A, Hess HD (2005). Supplementation of Acacia mearnsii tannins decreases methanogenesis and urinary nitrogen in forage-fed sheep. Aust. J. Agric. Res. 56:961-970. https://doi.org/10.1071/AR05022

• Callaway ES, Martin SA (1997). Effects of a Saccharomyces cerevisiae culture on ruminal bacteria that utilize lactate and digest cellulose. J. Dairy Sci. 80: 2035-2044. https://doi.org/10.3168/jds.S0022-0302(97)76148-4

• Chanjula P, Petcharat V, Cherdthong A. (2018). Rumen characteristics and feed utilization in goats fed with biologically treated oil palm fronds as roughage in a total mixed ration. 48: 1049-1056. https://doi.org/10.4314/sajas.v48i6.7

• Chaucheyras-Durand F, Chevaux E, Martin C, Forano E (2012). Use of yeast probiotics in ruminants: effects and mechanisms of action on rumen pH, fibre degradation, and microbiota according to the diet. Probiotic in Animals. 7: 119-152. http://dx.doi.org/10.5772/50192

• Chaucheyras-Durand F, Fonty G, Bertin G, Gouet P (1995). In vitro H2 utilization by a ruminal acetogenic bacterium cultivated alone or in association with an archaea methanogen is stimulated by a probiotic strain of Saccharomyces cerevisiae. Applied Environ. Microbiol. 61: 3466-3467

• Denev SA, Peeva TZ, Radulova P, Stancheva N, Staykova G, Beev G, Todorova P, Tchobanova S (2007). Yeast cultures in ruminant nutrition. Bulg. J. Agric. Sci. 13:357–374.

• Doležal P, Doležal J, Třináctý J (2005). The effect of Saccharomyces cerevisiae on ruminal fermentation in dairy cows. Czech J. Anim. Sci. 11: 503–510. https://doi.org/10.17221/4255-CJAS

• García E, López A, Zimerman M, Hernández O, Arroquy J, Nazareno M (2019). Enhanced oxidative stability of meat by including tannin-rich leaves of woody plants in goat diet Asian-Australas J. Anim. Sci. 32:1439-1447. https://doi.org/10.5713/ajas.18.0537

• Ginting PS, Simanihuruk K, Tarigan A, Pond KR (2018). Nutritional support for small ruminant development based on oil palm by-products. Wartazoa 28: 189-198.

• Goel G, Makkar HPS, Becker K (2008). Effects of Sesbania sesban and Carduus pycnocephalus leaves and Fenugreek (Trigonella foenum-graecum L.) seeds and their extracts on partitioning of nutrients from roughage- and concentrate-based feeds to methane. Anim. Feed Sci. Technol., 147: 72-89. https://doi.org/10.1016/j.anifeedsci.2007.09.010

• Goering HK, Van Soest PJ (1970). Forage fiber analyses (apparatus, reagents, procedures, and some applications). Agriculture handbook no. 379. United States Department of Agriculture, Washington DC, USA.

• Hau DK, Katipana NGF, Nulik J, Pohan A, Lailogo OT, Liem C (2004). Effect of probiotic on nitrogen retention, energy and growth of Bali cattle. Proceedings of the National Seminar on Technology and Veterinary Science, August 4-5, 2004, Bogor, Indonesia, pp: 91-96.

• Herawaty RN, Jamarun M, Zain A, Ningrat RWS. (2013). Effect of supplementation Saccharomyces cerevisiae and Leucaena leucocephala on low-quality roughage feed in beef cattle diet. Pak. J. Nutr. 12:182-184. http://dx.doi.org/10.3923/pjn.2013.182.184

• Jentsch W, Schweigel M, Weissbach F, Scholze H, Pitroff W, Derno M (2007). Methane production in cattle calculated by the nutrient composition of the diet. Arch. Anim. Nutr., 61: 10-19. https://doi.org/10.1080/17450390601106580

• Kamal R, Dutt T, Singh M, Nandan D, Patel M, Choudhary L. Agarwal N. Kumar S. Islam M. (2013). Effect of live Saccharomyces cerevisiae (NCDC-49) supplementation on growth performance and rumen fermentation pattern in local goat. J. Appl. Anim. Res. 41: 285-288. https://doi.org/10.1080/09712119.2013.782865

• Kamel HEM, Sekine J, El Waziry AM, Yacout MHM (2004). Effects of Saccharomyces cerevisiae on the synchronization of organic matter and nitrogen degradation and nitrogen degradation kinetics and microbial nitrogen synthesis in sheep fed Barseem hay (Trifolium alexandrinum). Small Ruminant Res. 52:211-216. https://doi.org/10.1016/j.smallrumres.2003.06.001

• Kumar S, Chigurupati D, Prasad S, Prasad RMV (2013). Effect of yeast culture (Saccharomyces cerevisiae) on the ruminal microbial population in buffalo bulls. Buff Bull. 32:116-119.

• Makkar HPS (2003). Effect and fate of tannins in ruminant animals, adaptation to tannins, andstrategies to overcome detrimental effects offeeding tannin-rich feeds. Small Ruminant Res. 49: 241–256. https://doi.org/10.1016/S0921-4488(03)00142-1

• Makkar HPS, Francis G, Becker K (2007). Bioactivity of phytochemicals in some lesser-known plants and their effects and potential applications in livestock and aquaculture production systems. Animal. 1:1371-1391. https://doi.org/10.1017/S1751731107000298

• Makkar HPS, Becker K, Abel H, Szegletti C (1995). Degradation of condensed tannins by rumen microbes exposed to quebracho tannins (QT) in rumen simulation technique (RUSITEC) and effects of QT on fermentative processes in the RUSITEC. J. Sci. Food Agric. 69: 495–500. https://doi.org/10.1002/jsfa.2740690414

• McLeod, MN (1974). Plant tannins-their role in forage quality. Nutr. Abst. Rev. 44: 803-815.

• Min BR, Barry TN, Attwood GT, McNabb WC (2003). The effect of condensed tannins on the nutrition and health of ruminants fed fresh temperate forages: a review. Anim. Feed Sci. Technol. 106: 3-19. https://doi.org/10.1016/S0377-8401(03)00041-5

• Natalello A, Biondi L, Campidonico L, Salami SA, Lanza M, Priolo A, Luciano G (2019). Intramuscular fatty acids in lambs supplemented with different tannin extracts. ASPA 23rd Congress Book of Abstracts, Ital. J. Anim. Sci. 18:26-27. https://doi.org/10.1080/1828051X.2019.1622269

• Ningrat RWS, Zain M, Erpomen, Suryani H (2017). Effect of doses and different sources of tannins on in vitro ruminal methane, volatile fatty acids production and on bacteria and protozoa populations. Asian J. Anim. Sci. 11: 47-53. http://dx.doi.org/10.3923/ajas.2017.47.53

• Ningrat RWS, Zain M, Erpomen, Putri EM, Makmur M (2019). Effects of Leucaena leucocephala supplementation to total mixed ration based on ammoniated rice straw on fiber digestibility and rumen fermentation characteristics in vitro. Int. J. Adv. Sci. Eng. Technol. 9: 916-921. http://dx.doi.org/10.18517/ijaseit.9.3.8009 12

• Nurdin E, Fitrimiwati (2018). The effect of the gambir (Uncaria gambir (hunt.) roxb.) leaves waste and white turmeric (Curcuma zedoaria) for the productivity, antioxidant content and mastitis condition of the fries holland dairy cows. IOP Conf. Ser.: Earth Environ. Sci. 119 012041. https://doi.org/10.1088/1755-1315/119/1/012041

• Patra AK (2010). Meta-analysis of effects of phytochemicals on digestibility and rumen fermentation characteristics associated with methanogenesis. J. Sci. Food Agric. 90: 2700–2708. https://doi.org/10.1002/jsfa.4143

• Piñeiro-Vázquez A, Canul-Solis J, Jiménez-Ferrer G, Alayón-Gamboa J, Chay-Canul A, Ayala-Burgos A, Aguilar-Pérez C, Ku-Vera J. (2018). Effect of condensed tannins from Leucaena leucocephala on rumen fermentation, methane production and population of rumen protozoa in heifers fed low-quality forage. Asian-Australas J. Anim. Sci. 31:1738-1746. https://doi.org/10.5713/ajas.17.0192

• Plata FP, Mendoza GD, Barcena-Gama JR, Gonzalez SM (1994). Effect of a yeast culture (Saccharomyces cerevisiae) on neutral detergent fiber digestion in steers fed oat straw based diets. Anim. Feed Sci. Tech. 49: 203-210. https://doi.org/10.1016/0377-8401(94)90046-9

• Prasetiyono BWHE, Subrata A, Tampoebolon BIM, Surono, Widiyanto (2018). In vitro ruminal degradability of soybean meal protein protected with natural tannin. IOP Conf. Ser: Earth Environ. Sci. 119 012016. https://doi.org/10.1088/1755-1315/119/1/012016

• Rivera-Mendez C, Plascencia A, Torrentera N, Zinn RA (2017). Effect of level and source of supplemental tannin on growth performance of steers during the late finishing phase. J. Appl. Anim. Res. 1:199-203. https://doi.org/10.1080/09712119.2016.1141776

• Riyanti L, Suryahadi, Evvyernie D (2016). In vitro fermentation characteristics and rumen microbial population of diet supplemented with Saccharomyces cerevisiae and rumen microbe probiotics. Med. Pet. 39:40-45. https://doi.org/10.5398/medpet.2016.39.1.40

• Sajati G, Prasetyo BWHE, Surono (2012). Influence of extrusion and protection of soybean by natural tannin on total gas and methane production in vitro. Animal Agricultural Journal, Vol. 1(1): 241-256.

• Sinz S, Marquardt S, Soliva C, Braun U, Liesegang A, Kreuzer M (2019). Phenolic plant extracts are additive in their effects against in vitro ruminal methane and ammonia formation Asian-Australas J Anim Sci. 32:966-976. https://doi.org/10.5713/ajas.18.0665

• Smith T, Mlambo V, Sikosana JLN, Maphosa V, Mueller-Harvey I, Owen E (2005). Dichrostachys cinerea and Acacia nilotica fruits as dry season feed supplements for goats in a semi-arid environment: summary results from a DFID funded project in Zimbabwe. Anim Feed Sci Technol. 122:149-157. https://doi.org/10.1016/j.anifeedsci.2005.04.004

• Steel RGD, Torrie JH (1993). Principles and procedures of statistics. McGraw-Hill Inc., New York, USA.

• Suryani H, Zain M, Jamarun N, Ningrat RWS (2015). The role of Direct Fed Microbials (DFM) Saccharomyces cerevisiae and Aspergillus oryzae on ruminant productivity: a Review. Jurnal Peternakan Indonesia. 17: 27-37. https://doi.org/10.25077/jpi.17.1.27-37.2015

• Suryani H, Zain M, Ningrat RWS, Jamarun N (2016). Supplementation of Direct Fed Microbials (DFM) on in vitro fermentability and degradability of ammoniated palm frond. Pak. J. Nutr. 15: 90-95. https://scialert.net/abstract/?doi=pjn.2016.89.94

• Suryani H, Zain M, Ningrat RWS, Jamarun N (2017). Effect of dietary supplementation based on an ammoniated palm frond with direct fed microbials and virgin coconut oil on the growth performance and methane production of Bali cattle. Pak. J. Nutr. 16: 599-604. http://dx.doi.org/10.3923/pjn.2017.599.604

• Steel RGD, Torrie JH (1980). Principles and procedure of statistics. McGraw-Hill Book Co. Inc., New York, USA.

• Tan HY, Sieo CC, Abdullah N, Liang JB, Huang XD Ho YW (2011). Effects of condensed tannins from Leucaena on methane production, rumen fermentation and populations of methanogens and protozoa in vitro. Anim. Feed Sci. Technol. 169: 185-193. https://doi.org/10.1016/j.anifeedsci.2011.07.004

• Tavendale MH, Meahger LP, Pacheco D, Walker N, Attwood GG, Sivakumaran S (2005). Methane production from in vitro rumen incubation with Lotus pondoculatus and Medicago sativa and effects of extracable condensed tannin fraction on methanogenesis. Anim. Feed Sci. and Technol. 123-124:403- 419. https://doi.org/10.1016/j.anifeedsci.2005.04.037

• Tilley JMA, Terry RA (1963). A two stage technique for the in vitro digestion of forage crops. Grass and Forage Sci. 18 : 104 – 111. https://doi.org/10.1111/j.1365-2494.1963.tb00335.x

• Whitley NC, Cazac D, Rude BJ, Jackson-O’Brien D, Parveen S (2009). Use of commercial Probiotics supplement in meat goat. J. Anim. Sci., 87: 723-728. https://doi.org/10.2527/jas.2008-1031

• Williams PEV, Newbold CJ (1990). Rumen probiosis: the effect of novel microorganisms on ruminal fermentation and ruminant productivity. In: Recent advances in Animal Nutrition (Ed. W. Haresign and D. J. A. Cole). Butterworths, London, England.

• Yeni G, Syamsu K, Suparno O, Mardliyati E, Muchtar, E (2014). Repeated extraction process of raw gambiers (Uncaria gambier Roxb.) for the catechin production as an antioxidant. IJAER. 9: 24565-24578.

• Zain M, Sutardi T, Suryahadi, Ramli N (2008). Effect of defaunation and supplementation methionine hydroxy analogue and branched chain amino acid in growing sheep diet based on palm press fiber ammoniated. Pak. J. Nutr. 7: 813-816. http://dx.doi.org/10.3923/pjn.2008.813.816

• Zain M, Jamarun N, Arnim A, Ningrat RWS, Herawaty R. (2011). Effect of yeast (Saccharomyces cerevisiae) on fermentability, microbial population, and digestibility of low-quality roughage in vitro. Arch. Zootech. 14: 51-58.

• Zain M, Rahman J, Khasrad, Erpomen (2016). Supplementation of Saccharomyces cerevisiae and Sapindus rarak in diet based of oil palm frond (OPF) on nutrient digestibility and daily weight gain of goat. Asian J. Anim. Vet. Adv., 11: 314-318. http://dx.doi.org/10.3923/ajava.2016.314.318

• Zahari MW, Abu Hassan O, Wong HK, Liang JB (2003). Utilization of oil palm frond-base diets for beef and dairy production in Malaysia. Asian-Aust. J. Anim. Sci. 16: 625-634. https://doi.org/10.5713/ajas.2003.625

• Zhao M, Di LF, Tang ZY, Jiang W, Li CY (2019). Effect of tannins and cellulase on growth performance, nutrients digestibility, blood profiles, intestinal morphology and carcass characteristics in Hu sheep. Asian-Australas J Anim Sci. 32:1540-1547. https://doi.org/10.5713/ajas.18.0901

• Zhu W, Wei, Z, Xu N (2017). Effects of Saccharomyces cerevisiae fermentation products on performance and rumen fermentation and microbiota in dairy cows fed a diet containing low quality forage. J Animal Sci Biotechnol 8: 1-9. https://doi.org/10.1186/s40104-017-0167-3