Review Article

Alternative Strategies of Plant Metabolite Secondary “Tannin” for Methane Emissions Reduction on Ruminant Livestock a Reviews of the Last 5 Years Literature

Zein Ahmad Baihaqi1,2, Irkham Widiyono3*, Bambang Suwignyo4, Amado A. Angeles5

1Doctoral Program Veterinary Science, Faculty of Veterinary Medicine, Universitas Gadjah Mada, Yogyakarta, Indonesia; 2Department of Animal Nutrition, Faculty of Agriculture, Universitas Islam Kadiri, Kediri, Indonesia; 3Department of Internal Medicine, Faculty of Veterinary Medicine, Universitas Gadjah Mada, Yogyakarta, Indonesia; 4Department of Animal Nutrition and Feed Science, Faculty of Animal Science, Universitas Gadjah Mada, Yogyakarta, Indonesia; 5Animal and Dairy Sciences Cluster College of Agriculture, University of the Philippines Los Banos, Philippines.

Received | March 01, 2021; Accepted | June 30, 2021; Published | February 15, 2022

*Correspondence | Irkham Widiyono, Department of Internal Medicine, Faculty of Veterinary Medicine Universitas Gadjah Mada, Yogyakarta, Indonesia; Email: [email protected]

Citation | Baihaqi ZA, Widiyono I, Suwignyo B, Angeles AA (2022). Alternative strategies of plant metabolite secondary “Tannin” for methane emissions reduction on ruminant livestock a reviews of the last 5 years literature. Adv. Anim. Vet. Sci. 10(3): 599-606.

DOI | http://dx.doi.org/10.17582/journal.aavs/2022/10.3.599.606

ISSN (Online) | 2307-8316

 

INTRODUCTION

Livestock production is one of the major contributors to greenhouse gases such as methane (CH4) and carbon dioxide (CO2). These gases contribute greatly to global warming, environmental degradation and pollution. Livestock production system is responsible for 18% CH4 and 9% CO2 productions of all greenhouse gases emissions. Methane has a greater global warming effect (about 23 times) more than CO2 (Ugbogu et al., 2019). Lakhani and Lakhani (2018) stated that methane makes up 16% of total global GHG emissions which is probably the second most important gas after CO2 contributing to global warming. Methane has 23 times more global warming potential than carbon dioxide. Naumann et al. (2015) added that stated that ethane emissions from ruminant livestock contribute to total anthropogenic greenhouse gas emissions and reduce metabolizable energy intake by the animal.

In ruminants, approximately 95.5% of CH4 generation is produced by fermentation of feed in the rumen (Lakhani and Lakhani, 2018). Dairy cows are responsible for significant emissions of centrifuge of methane (CH4) and produce nitrous oxide (N2O) and ammonia (NH3) gas from manure (Duval et al., 2016). Livestock production encounters a great challenge of increasing production to meet global demand for agricultural products and at the same time reduces environmental impact. Many researchers have reported the effects of substituting phytoconstituents such as tannins and saponins as chemical feed additives to modify rumen fermentation (Ugbogu et al., 2019).

Ku-vera et al. (2020) stated that plant secondary metabolites are shown to rationally modulate the rumen microbiome and modify its function, reduce feed energy loss as methane in ruminants, rumen microbial species increase protein and degradation of fiber in a tropical feed plant species. Dermitas et al. (2018) stated that effects of plant secondary metabolites on ruminal fermentation are favorable if they increase or do not change VFA production (or with a desirable change in molar proportions of VFA) and feed digestibility while they decrease ammonia concentration and methane production. Ugbogu et al. (2019) added that natural plant products (NPP) or secondary metabolites have the potential to improve rumen fermentation, reduce loss of feed energy, improve animal health and productivity, increase animal lifetime performance, and reduce greenhouse gases production-CH4 and CO2 during animals’ production. Rira et al. (2019) emphasized that secondary plant metabolites can be used as feed additives to reduce CH4 production and to consequently mitigate greenhouse-gases emission. This study will focus on providing information on the last 5 years related to the role of active tannin plant compounds as an alternative to reduce ruminant livestock methane gas production. It is hoped that the results of this study can be used as a reference in conducting research to emphasize the upcoming methane gas production.

Alternative treatment to reduce methan production

Methane (CH4) emissions caused by ruminants arise from fermentation of feed in the rumen. Methane is an important cause of the greenhouse effect and at the same time causes energy loss from livestock so that it can cause a decrease in productivity. Because methane emissions are affected by feed, ruminant nutritionists are invited to focus their studies on feed strategies that can reduce methane production (Adegbeye et al., 2019). Plant resources such as legumes or agro-industrial wastes contain condensed tannins consisting of flavon-3-ol polymer units that have the potential to suppress methane production (Mueller-Harvey et al., 2019). Some studies have shown that the use of condensed tannins generated diets has decreased methane emissions (Piñeiro-Vázquez et al., 2018).

Hoehn et al. (2018) emphasized that one of the well-known types of plant secondary metabolite compounds helps the production of livestock, condensed tannins, which are polyphenol compounds having the ability to modulate rumen fermentation, suppress the production of methane. Adejoro et al. (2019) asserted that tannins have been shown to be important phytochemicals in ruminant production due to various biological activities and reduced emissions of enteric methane in ruminant animals. Zeller et al. (2019) added that the positive impact of the potential active plant compounds in the form of tannins on plants could reduce methane emissions.

Hoehn et al. (2018) emphasized that one of the well-known types of plant secondary metabolite compounds helps the production of livestock, condensed tannins, which are polyphenol compounds having the ability to modulate rumen fermentation, suppress the production of methane. Adejoro et al. (2019) asserted that tannins have been shown to be important phytochemicals in ruminant production due to various biological activities and reduced emissions of enteric methane in ruminant animals. Zeller (2019) added that the positive impact of the potential active plant compounds in the form of tannins on plants could reduce methane emissions.

Tannins effect on reduction of methan production

Recent developments regarding the evaluation of the content of secondary metabolites (tannins) in plants and/or agricultural industrial waste in an innovative effort to suppress methane production in ruminants in the last 5 years are shown in Table 1. The use of plant secondary metabolites as a natural alternative to reduce the impact of livestock on the environment continues to attract great interest globally (Chen et al., 2015). Natural strategies to reduce methane production are utilizing tannin sources in plants. Tannins are classified into hydrolyzed tannins (HT) and condensed tannins (CT). The reduction in CH4 yield (g CH4 per kg DMI) with tannin utilization has been ascribed to direct negative impacts on microbial populations (Pineiro-Vazquez et al., 2015). But, Sliwiński et al. (2002) reported that tannins did not show any effect on methanogenesis or even CH4 enhanced production in sheep. These differences could be the result of dosage, type and source of tannins or the type of feed. Patra et al. (2011) stated that molecular weight is a key factor for its effect on digestive enzymes and microbes in the rumen. Low molecular weight tannins could be more effective inhibitors of microbes, including methanogens, compared with high molecular weight tannins.

 

Table 1: Tannin effect for CH4 reduction in rumen.

No.	Kind of plant	Test system	Doses	Effect on CH4	Reference
1	L. leucocephala	In vitro	Supplemented with 30.0% on feed basis	Decrease ,25.8 L kg−1	Albores-Moreno et al., 2019
	P. piscipula			Decrease, 29.5 L kg−1
	N. emargiata			Decrease, 30.6 L kg−1
	T. amygdalifolia			Decrease, 31.8 L kg−1
2	B. variegata	In vitro	Supplemented 1%	Decrease, 34.82 mmoles	Deuri et al., 2019
3.	P. granatum T. undulata	In vivo	2% of dry matter intake	Decrease, 46% Decrease, 42%	Hundal et al., 2019
4	A. julibrissin	In vitro	500 mg	2.55 w/0 PEG	Bouazza et al., 2019
	A. nilotica			1.72 w/0 PEG
	P. granatum			2.63 w/0 PEG
	V. faba A. herba-alba			4.92 w/0 PEG 1.63 w/0 PEG
	A. halimus			0.93 w/0 PEG
	C. azel			0.13 w/0 PEG
5.	A. mearnsii	In vitro	5% DM	reduced by 7% to 9%	Sinz et al., 2019
	V. vinifera			reduced by 7% to 9%
	C. sinensis			reduced by 7% to 9%
6	Condensed tannins	In vivo	0	2.99 % of GE intake	Ebert et al., 2017
	(By-Pro; Silvateam		0, 0.5	Increase 3.12% of GE intake
	USA, Ontario, CA)		1	Increase 3.09% of GE intake
7.	F. benghalensis A. heterophyllus	In vivo	10 parts w/w on concentrate	Decrease, 19.5 CH4 (g/d) Decrease, 19.4 CH4 (g/d)	Malik et al., 2017
	A. indica			Decrease, 18.1 CH4 (g/d)
8.	A. mearnsii	In vivo	120 g extract	Decreased 32%	Alves et al., 2017
9.	G. biloba	In vitro	1.6% extract	Decreased 53%	Oh et al., 2017
10.	C. papaya	In vitro	5 mg/0.25g DM	Decrease 13%	Jafari et al., 2017
			10 mg/0.25g DM	Decrease 16%
			15 mg/0.25g DM	Decrease 34%
11.	C. sinensis	In vitro	0.8%	Decrease 48.55 ml/gm	Jadhav et al., 2016
12.	Quebracho and chestnut trees	In vivo	0.45% tannin	56 cow−1 day−1	Duval et al., 2016
			1.8% tannin	48 cow−1 day−1
13.	Mimosa	In vitro	38 mg	23%	Jayanegara et al., 2015
	Quebraco			27%
	Chesnut			23%
	Sumac			20%
14.	A. taxiformis	In vitro	2% of the control OM (w/w)	12.32 mL g−1 OM	Vucko et al., 2017
15.	O. viciifolia	In vitro	40 g/kg of DM	19.4 %	Hatew et al., 2016
	(Cotswold Common)		80 g/kg of DM	16.1 %
			120 g/kg of DM	12.9 %
16.	D. paniculatum	In vitro	45%	Decrease 65.6%	Nauman et al., 2015
	S. lespedeza		45%	Decrease 24.2%
17.	Porphyra sp	In vivo	10% of DM	Not influenced CH4	Lind et al., 2020
18.	C. avellana	In vitro	30.4% basal diet	1.31 mmol/g DM	Niderkorn et al., 2020
	O. viciifolia		8.2% basal diet	1.34 mmol/g DM
No.	Kind of plant	Test system	Doses	Effect on CH4	Reference
19.	Banana pseudo stems	In vitro	25.6 g squeezed and 26.5 g unsqueezed	12.5%	Pan et al., 2020
20.	L. leucocephala	In vitro	2 mg/100 mg DM	12.5	Petlum et al., 2019
			6 mg/100 mg DM	5.8
	A. indica		2 mg/100 mg DM	3.3
			4 mg/100 mg DM	1.7
21.	A. mearnssii	In vivo	30 g Acacia/kg of dietary DM	Decrease, 0.16 g/kg DM	Denninger et al., 2020
22.	M. tenuiflora	In vivo	30 g/kg DM	Decrease, 35.9 L/day	Lima et al., 2019
23.	M. stenopetala	In vitro	extract 200 mg	51.66 ml g-1 DM	Tirfessa and Adugna, 2019
	A. nilotica		extract 200 mg	18.33 ml g-1 DM
24.	O. vocoofolia	In vitro	500 mg	3.7 mL/mmol	Rufino-Moya et al., 2019
	H. coronarium		500 mg	3.4 mL/mmol
25.	A. mearnssii	In vivo	50 g/kg feed	Decrease, 19%	Adejoro et al., 2019
26.	S. cumini	In vivo	50% basal diet	Reduction, 18.9%	Baruah et al., 2019
	M. bombycina		50% basal diet	Reduction, 20.9%
27.	Chestnut and quebracho mix	In vivo	1.5%	Decrease, 20.6 g/kg DMI	Aboagye et al., 2018
28.	G. march	In vivo	34.9 mg CT	Decrease, 33.03 mL/g DM	Hixson et al., 2018
29.	D. paniculatum	In vitro	508 nm	4.9 g/kg DM	Naumann et al., 2018
	L. stuevei		543 nm	4.9 g/kg DM
	L. cuneata		543 nm	15.1 g/kg DM
	M. strigillosa		547 nm	7.6 g/kg DM
	D. illinoensis		547 nm	24.9 g/kg DM
	N. lutea		547 nm	19.7 g/kg DM
	L. retusa		547 nm	40.7 g/kg DM
	A. angutissima		547 nm	0.6 g/kg DM
	A. angustissima STX		538 nm	0.8 g/kg DM
30.	Lespedeza	In vivo	1.46 kg/d DM	1.36 Mj/d	Liu et al., 2018
			1.23 kg/d DM	0.76 Mj/d
			1.30 kg/d DM	0.84 Mj/d
			1.18 kg/d DM	0.71 Mj/d
			1.32 kg/d DM	0.71 Mj/d
			1.10 kg/d DM	0.66 Mj/d
			1.02 kg/d DM	0.65 Mj/d
			1.20 kg/d DM	0.68 Mj/d
			1.01 kg/d DM	0.68 Mj/d

 

Hydrolyzed and condensed tannins appear to have a role in limiting methane production, but the research currently has focused largely on CT because of their wide distribution among forages. Most studies are limited to dose-response information, and there is almost no information about the structure of tannins or chemical properties (Mueller-Harvey, 2006). Condensed tannin is a diverse class of compounds, in which efforts to suppress the production of methanogen depend on the dose of administration and focus more on the structure of CT, the composition and ability of CT extraction to put more emphasis on methanogenic (Huyen et al., 2016). However, Carrasco et al. (2017) have another opinion, where the decrease in methane production caused by methanogenic bacterial using addition of a mixture of HT and CT, compared with HT itself or CT itself. Meanwhile, Rira et al. (2019) found that HT and CT similarly showed inhibition of CH4 production, but HT was not followed by adverse effects of digestive rumen fermentation while CT showed an adverse effect on rumen fermentation. In addition, Hatew et al. (2016) also stated that CT forming or structural features need to get focus, including the size of the polymers and the structural characteristics of flavanols. Nauman et al. (2015) added that the structural components of CT are not commonly determined, not many of them have discovered the properties of CT that play a good role in suppressing methane production.

The role of active plant compounds (tannins) in feed nutrition varies and is influenced by several factors such as tannin concentrations in feed, biological characteristics of tannin compounds, animal species, prolonged and adaptation effects of feed (Archimède et al., 2016). Animut et al. (2008) explained that tannin was also associated with inhibition of the growth of the methane-producing community through the tannin action of their functional proteins, resulting in bacteriostatic and bactericidal effects or indirectly there is defaunating in methanogen-related protozoan populations. Naumann et al. (2015) related to the correlation of antioxidants on methane production. CT galloylation has a correlation increasing the antioxidant activity of flavan-3-ols. A strong nonlinear correlation was observed between antioxidant activity (TE per g of plant tissue) and methane production (g CH4 per g of plant tissue).

The effectiveness of active plant compounds in the mission of reducing methane production is also influenced by animal species. Roque et al. (2019) stated that the utilization of the Asparagopsis genus plant which was included in 1% of the total feed of dairy cows succeeded in reducing 67% of energy CH4 emissions, while Li et al. (2018) stated that the utilization of plants with the genus was tested on sheep with concentrations of 0.5%, 1%, 2 % and 3% succeeded in reducing enteric CH4 to 80% compared to control cattle. Addition of tannin to the feed does not always have an impact on reducing methane production. Lima et al. (2019) stated that in vivo treatment in sheep by adding tannin 30g/kg DM did not influence the decreasing of methane production L/day (P = 0.14). Lind et al. (2020) emphasized that the addition of clover silage (CLO), soybean meal (SOY) or Porphyra sp. (POR) does not contribute to the decrease in methane production through in vitro and in vivo in sheep.

The availability of tannins in plants can be used as an alternative to reduce methane production, in a way suppress H2 availability, and reduce fiber digestion (Vucko et al., 2017), and/or maximizing the content of active plant compounds in the form of condensed tannins to influence methanogenic archaea populations and their activities in the rumen (Saminathan et al., 2016). Bouazza et al. (2019) found that legume plant species in Algeria Albizia julibrissin (pods), Acacia nilotica (pods), Punica granatum (leaves and pericarp), Vicia faba (leaves), Artemisia herba-alba (aerial part), Attriplexhalimus (leaves) and Calligonum azel (bark) have been proven to have reduced methane to 0.13 w/o PEG. Niderkorn et al. (2020) stated that condensed tannins in C. avellena with a concentration of 30.4% from the basal diet decreased the production of methane 1.31 mmol/g DM DM. Denninger et al. (2020) also found that the addition of Acacia mearnssii bark at a concentration of 30 g Acacia/kg of DM in vitro decreased methane production of 0.16 g/kg DM. Albores-moreno et al. (2019) explained that supplementation with L. leucocephala, P. piscipula, N. emargiata and T. amygdalifolia in ruminant diets was based on decreased production of enteric methane by 15.6 to 31.6%. Sinz et al. (2019) stated that tannins on acacia, grape seed and green tea plants provide reduced methane formation 7% to 9% through in vitro.

CONCLUSIONS AND RECOMMENDATIONS

The conclusion from the last 5 years review results that tannins remain proven to emphasize methane production through in vitro and in vivo, both CT and HT. The use of HT did not have an effect on rumen digestion fermentation, but until the latest development of CT, it has been associated with many treatments for decreased methane production. The success of suppressing methane production with the use of active tannin compounds is influenced by the number of doses and types of tannins, the content of tannins in plants, and the types of animals whose methane production will be suppressed.

Novelty Statement

This review addresses the role of tannins in the plants as an alternative natural strategy to reduce methane emission production in ruminants reported in the last 5 years literature.

Author’s Contribution

ZAB and AAA wrote the manuscript. IW and BS edited the final version of the manuscript. All authors contributed to manuscript revision, intellectual content, and approved the manuscript for publication.

Conflict of interest

The authors have declared no conflict of interest.

REFERENCES

Aboagye IA, Masahito O, Alejandro RC, Karen MK, Alan DI, Karen AB (2018). Effects of hydrolyzable tannin with or without condensed tannin on methane emissions, nitrogen use, and performance of beef cattle fed a high-forage diet. J. Anim. Sci., 96: 5276–5286. https://doi.org/10.1093/jas/sky352

Adegbeye MJ, Elghandour MMY, Monroy JC, Abegunde TO, Salem AZM, Barbabosa-Pliego A, Faniyi TO (2019). Potential influence of Yucca extract as feed additive on greenhouse gases emission for a cleaner livestock and aquaculture farming. A review. J. Cleaner Prod., https://doi.org/10.1016/j.jclepro.2019.118074

Adejoro FA, Hassen A, Thantsha MS (2019). Characterization of starch and gum arabic-maltodextrin microparticles encapsulating acacia tannin extract and evaluation of their potential use in ruminant nutrition. Asian Austral. J. Anim. Sci., 32: 977–987. https://doi.org/10.5713/ajas.18.0632

Albores-Moreno S, Alayón-Gamboa JA, Miranda-Romero LA, Alarcón-Zúñiga B, Jiménez-Ferrer G, Ku-Vera JC, Piñeiro- Vázquez AT (2019). Effect of tree foliage supplementation of tropical grass diet on in vitro digestibility and fermentation, microbial biomass synthesis and enteric methane production in ruminants. Trop. Anim. Health Prod., 51: 893–904. https://doi.org/10.1007/s11250-018-1772-7

Alves TP, Dall-Orsoletta AC, Ribeiro-Filho HMN (2017). The effects of supplementing Acacia mearnsii tannin extract on dairy cow dry matter intake, milk production, and methane emission in a tropical pasture. Trop. Anim. Health Prod., 49: 3-8. https://doi.org/10.1007/s11250-017-1374-9

Animut G, Puchala R, Goetsch AL (2008). Methane emission by goats consuming different sources of condensed tannins. Anim. Feed Sci. Tech., 144: 228-241. https://doi.org/10.1016/j.anifeedsci.2007.10.015

Archimède H, Rira M, Barde DJ, Labirin F, Marie-Magdeleine C, Calif B., Periacarpin F, Fleury J, Rochette Y, Morgavi DP (2016). Potential of tannin-rich plants, Leucaena leucocephala, Glyricidia sepium and Manihot esculenta, to reduce enteric methane emissions in sheep. J. Anim. Physiol. Anim. Nutr., 100: 1149–1158. https://doi.org/10.1111/jpn.12423

Baruah L, Pradeep KM, Atul PK, Priyal G, Arindam D, Raghavendra B (2019). Rumen methane amelioration in sheep using two selected tanniferous phyto-leaves. Carbon Manage., 10(3): 299-308. https://doi.org/10.1080/17583004.2019.1605480

Bouazza L, Boufennara S, Bensaada M, Zeraib A, Rahal K, Saro C, Jose M, Lo´pez RS (2019). In vitro screening of Algerian steppe browse plants for digestibility, rumen fermentation profile and methane mitigation. Agrofor. Syst., 94(4): 214. https://doi.org/10.1007/s10457-019-00408-1

Carrasco JMD, Cabral C, Redondo LM, Viso NDP, Colombatto D, Farber MD, Miyakawa MEF (2017). Impact of chestnut and quebracho tannins on rumen microbiota of bovines. BioMed. Res. Int., 2017: 1–11. https://doi.org/10.1155/2017/9610810

Chen D, Chen X, Tu Y, Wang B, Lou C, Ma T, Diao QE (2015). Effect of mulberry leaf flavonoid and resveratrol on methane emission and nutrient digestion in sheep. Anim. Nutr., 1: 362–367. https://doi.org/10.1016/j.aninu.2015.12.008

Denninger TM, Schwarm A, Birkinshaw A, Terranova M, Dohme-Meier F, Münger A, Eggerschwiler B, Bapst S, Wegmann M, Clausse KM (2020). Immediate effect of Acacia mearnsii tannins on methane emissions and milk fatty acid profiles of dairy cows. Anim. Feed Sci. Tech., 223: 114388. https://doi.org/10.1016/j.anifeedsci.2019.114388

Dermitas A, Özturk H, Piskin I (2018). Overview of plant extracts and plant secondary metabolites as alternatives to antibiotics for modification of ruminal fermentation. Ankara Üniv. Vet. Fak. Derg., 65: 213-217. https://doi.org/10.1501/Vetfak_0000002849

Deuri P, Sood N, Wadhwa M, Bakshi MPS, Salem AZM (2019). Screening of tree leaves for bioactive components and their impact on in vitro fermentability and methane production from total mixed ration. Agrofor. Syst., 94: 1455–1468. https://doi.org/10.1007/s10457-019-00374-8

Duval BD, Matias A, Michel W, Peter AV, Powell JM (2016). Potential for reducing on-farm greenhouse gas and ammonia emissions from dairy cows with prolonged dietary tannin additions. Water Air Soil Pollut., 227: 329. https://doi.org/10.1007/s11270-016-2997-6

Ebert PJ, Bailey EA, Shreck AL, Jennings JS, Cole NA (2017). Effect of condensed tannin extract supplementation on growth performance, nitrogen balance, gas emissions, and energetic losses of beef steers. J. Anim. Sci., 95 (3):1345-1355. https://doi.org/10.2527/jas2016.0341

Hatew B, Stringano E, Mueller-Harvey I, Hendriks WH, Carbonero CH, Smith LM, Pellikaan WF (2016). Impact of variation in structure of condensed tannins from sainfoin (Onobrychis viciifolia) on in vitro ruminal methane production and fermentation characteristics. J. Anim. Physiol. Anim. Nutr., 100: 348–360. https://doi.org/10.1111/jpn.12336

Hixson JL, Zoey D, Joy V, Philip EV, Paul AS, Eric NW (2018). Exploiting compositionally similar grape marc samples to achieve gradients of condensed tannin and fatty acids for modulating in vitro methanogenesis. Molecules, 23: 1793. https://doi.org/10.3390/molecules23071793

Hoehn AN, Titgemeyer EC, Nagaraja TG, Drouillard JS, Miesner MD, Olson KC (2018). Effects of high condensed-tannin substrate, prior dietary tannin exposure, antimicrobial inclusion, and animal species on fermentation parameters following a 48 h in vitro incubation. J Anim Sci. 96(1):343-353. https://doi.org/10.1093/jas/skx018. PMID: 29365124; PMCID: PMC6140839

Hundal JS, Singh I, Wadhwa M, Singh C, Uppal C, Kaur G (2019). Effect of Punica granatum and Tecomella undulata supplementation on nutrient utilization, enteric methane emission and growth performance of Murrah male buffaloes. J. Anim. Feed Sci., 28(2): 110–119. https://doi.org/10.22358/jafs/109237/2019

Huyen NT, Fryganas C, Uittenbogaard G, Mueller-Harvey I, Verstegen MWA, Hendriks WH, Pellikaan WF (2016). Structural features of condensed tannins affect in vitro ruminal methane production and fermentation characteristics. J. Agric. Sci., 154: 1474–1487. https://doi.org/10.1017/S0021859616000393

Jadhav RV, Kannan A, Bhar R, Sharma OP, Gulati A, Rajkumar K, Mal G, Singh B, Verma MR (2016). Effect of tea (Cammelia sinensis) seed saponins on in vitro rumen fermentation, methane production and true digestibility at different forage to concentrate ratios. J. Appl. Anim. Res., 46(1): 118-124. https://doi.org/10.1080/09712119.2016.1270823

Jafari S, Goh YM, Rajion MA, Jahromi MF, Ebrahimi M (2017). Papaya (Carica papaya) leaf methanolic extract modulates in vitro rumen methanogenesis and rumen biohydrogenation. Anim. Sci. J. 88(2):267-276. https://doi.org/10.1111/asj.12634

Jayanegara A, Goel G, Makkar PSH, Becker K (2015). Divergence between purified hydrolysable and condensed tannin effects on methane emission, rumen fermentation and microbial population in vitro. Anim. Feed Sci. Technol., 209: 60–68. https://doi.org/10.1016/j.anifeedsci.2015.08.002

Ku-Vera JC, Jiménez-Ocampo R, Valencia-Salazar SS, Montoya-Flores MD, Molina-Botero IC, Arango J, Gómez-Bravo CA, Aguilar-Pérez CF, Solorio-Sánchez FJ (2020). Role of Secondary Plant Metabolites on Enteric Methane Mitigation in Ruminants. Front. Vet. Sci. 7:584. https://doi.org/10.3389/fvets.2020.00584

Lakhani N, Lakhani P (2018). Plant secondary metabolites as a potential source to inhibit methane production and improve animal performance. Int. J. Chem. Stud., 6(3): 3375-3379.

Li X, Norman HC, Kinley RD, Laurence M, Wilmot M, Bender H, de Nys R, Tomkins N (2018). Asparagopsis taxiformis decreases enteric methane production from sheep. Anim. Prod. Sci., 58(4): 681–688. https://doi.org/10.1071/AN15883

Lima PR, Apdini T, Freire AS, Santana AS, Moura LML, Nascimento JCS, Rodrigues J, Dijkstr AF, Garcez NMAÁ, Queiroz- Menezes DR (2019). Dietary supplementation with tannin and soybean oil on intake, digestibility, feeding behavior,ruminal protozoa and methane emission in sheep. Anim. Feed Sci. Tech., 249: 10–17. https://doi.org/10.1016/j.anifeedsci.2019.01.017

Lind V, Weisbjerg MR, Jørgensen GM, Fernandez-Yepes JE, Arbesú L, Molina- Alcaide E (2020). Ruminal fermentation, growth rate and methane production in sheep fed diets including white clover, soybean meal or Porphyra sp. Animal, 10(1): 79. https://doi.org/10.3390/ani10010079

Liu HY, Puchala R, LeShure S, Gipson TA, Flythe MD, Goetsch AL (2018). Effects of lespedeza condensed tannins alone or with monensin, soybean oil, and coconut oil on feed intake, growth, digestion, ruminal methane emission and heat energy by yearling Alpine doelings. J. Anim. Sci., https://doi.org/10.1093/jas/sky404.1033

Malik PK, Kolte AP, Baruah L, Saravanan M, Bakshi B, Bhatta R (2017). Enteric methane mitigation in sheep through leaves of selected tanninniferous tropical tree species. Livest. Sci., 200: 29e34. https://doi.org/10.1016/j.livsci.2017.04.001

Mueller-Harvey I (2006). Unravelling the conundrum of tannins in animal nutrition and health. J. Sci. Food Agric., 86: 2010–2037. https://doi.org/10.1002/jsfa.2577

Mueller-Harvey I, Bee G, Dohme-Meier F, Hoste H, Karonen M, Kolliker R, Lüscher A, Niderkorn V, Pellikaan WF, Salminen JP, Skot L, Smith LMJ, Thamsborg SM, Totterdell P, Wilkinson I, Williams AR, Azuhnwi BN, Baert N, Grosse BA, Copani G, Desrues O, Drake C, Engstrom M, Fryganas C, Girard M, Huyen NT, Kempf K, Malisch C, Mora-Ortiz M, Quijada J, Ramsay A, Ropiak HM, Waghorn GC (2019). Benefits of condensed tannins in forage legumes fed to ruminants: importance of structure, concentration and diet composition. Crop. Sci., 59: 885–961. https://doi.org/10.2135/cropsci2017.06.0369

Naumann HD, Lambert BD, Armstrong SA, Fonseca MA, Tedeschi LO, Muir JP (2015). Effect of replacing alfalfa with panicled- tick clover or sericea lespedeza in cornalfalfa- based substrates on in vitro ruminal methane production. J. Dairy Sci., 98: 3980–3987. https://doi.org/10.3168/jds.2014-8836

Naumann HD, Rebecka S, Aira R, Sonia EM, Wayne EZ, Laurie AR, Jamison TR, Michael LS, Ann EH (2018). Relationships between structures of condensed tannins from Texas legumes and methane production during in vitro rumen digestion. Molecules, 23: 2123. https://doi.org/10.3390/molecules23092123

Niderkorn V, Barbier E, Macheboeuf D, Torrent A, Mueller-Harvey I, Hoste H (2020). In vitro rumen fermentation of diets with different types of condensed tannins derived from sainfoin (Onobrychis viciifolia Scop.) pellets and hazelnut (Corylus avellana L.) pericarps. Anim. Feed Sci. Tech., 259: 114357. https://doi.org/10.1016/j.anifeedsci.2019.114357

Oh S, Shintani R, Koike S, Kobayashi Y (2017). Ginkgo fruit extract as an additive to modify rumen microbiota and fermentation and to mitigate methane production. J. Dairy Sci., 100: 192334. https://doi.org/10.3168/jds.2016-11928

Pan S, Yue C, Lang Z, Zhenchong L, Liqin D, Yutuo W (2020). Evaluation of squeezing pretreatment for improving methane production from fresh banana pseudo-stems. Waste Manage., 102: 900–908. https://doi.org/10.1016/j.wasman.2019.12.011

Patra AK, Kamra DN, Bhar R, Kumar R, Agarwal N (2011). Effect of Terminalia chebula and Allium sativum on in vivo methane emission by sheep. J. Anim. Physiol. Anim. Nutr. (Berl.), 95(2): 187-191. https://doi.org/10.1111/j.1439-0396.2010.01039.x

Petlum A, Paengkoum P, Liang JB, Vasupen K, Paengkoum S (2019). Molecular weight of condensed tannins of some tropical feed-leaves and their effect on in vitro gas and methane production. Anim. Prod. Sci., 59: 2154–2160. https://doi.org/10.1071/AN17749

Pineiro-Vazquez AT, Canul-Solís JR, Alayón-Gamboa JA, Chay-Canul AJ, Ayala-Burgos J, AguilarPérez CF, Solorio-Sánchez FJ, Ku-Vera JC (2015). Potential of condensed tannins for the reduction of emissions of enteric methane and their effect on ruminant productivity. Arch. Med. Vet., 47: 263–272. https://doi.org/10.4067/S0301-732X2015000300002

Piñeiro-Vázquez AT, Jiménez-Ferrer G, Alayon-Gamboa JA, Chay-Canul AJ, Ayala- Burgos AJ, Aguilar-Pérez CF, Ku-Vera JC (2018). Effects of quebracho tannin extract on intake, digestibility, rumen fermentation, and methane production in crossbred heifers fed low quality tropical grass. Trop. Anim. Health Prod., 50: 29–36. https://doi.org/10.1007/s11250-017-1396-3

Rira M, Diego PM, Lucette G, Sihem D, Ines S, Michel D (2019). Methanogenic potential of tropical feeds rich in hydrolyzable tannins. J. Anim. Sci., 97: 2700–2710. https://doi.org/10.1093/jas/skz199

Roque MB, Salwen JK, Kinley R, Kebrea E (2019). Inclusion of Asparagopsis armata in lactating dairy cows’diet reduces enteric methane emission by over 50 percent. J. Clean. Prod., 234: 132–138. https://doi.org/10.1016/j.jclepro.2019.06.193

Rufino-Moya PJ, Blanco M, Bertolína JR, Joya M (2019). Effect of the method of preservation on the chemical composition and in vitro fermentation characteristics in two legumes rich in condensed tannins. Anim. Feed Sci. Tech., 251: 12–20. https://doi.org/10.1016/j.anifeedsci.2019.02.005

Saminathan M, Sieo CC, Gan HM, Abdullah N, Wong CMVL, Ho YW (2016). Effects of condensed tannin fractions of different molecular weights on population and diversity of bovine rumen methanogenic archaea in vitro, as determined by high-throughput sequencing. Anim. Feed Sci. Tech., 216: 146–160. https://doi.org/10.1016/j.anifeedsci.2016.04.005

Sinz S, Marquardt S, Soliva CR, Braun U, Liesegang A, Kreuzer M (2019). Phenolic plant extracts are additive in their effects against in vitro ruminal methane and ammonia formation. Asian Austral. J. Anim. Sci., 32(7): 966-976. https://doi.org/10.5713/ajas.18.0665

Sliwiński BJ, Kreuzer M, Wettstein HR, Machmüller A (2002). Rumen fermentation and nitrogen balance of lambs fed diets containing plant extracts rich in tannins and saponins, and associated emissions of nitrogen and methane. Arch. Tierernahr., 56(6): 379-392. https://doi.org/10.1080/00039420215633

Tirfessa G, Adugna T (2019). Comparative evaluation of chemical composition, in vitro fermentation and methane production of selected tree forages. Agrof. Syst., https://doi.org/10.1007/s10457-019-00391-7

Ugbogu EA, Mona MMYE, Vi OI, German RB, Ofelia MM, Uche OA, Okezie E, Abdelfattah ZMS (2019). The potential impacts of dietary plant natural products on the sustainable mitigation of methane emission from livestock farming. J. Clean. Prod., 213: 915-925. https://doi.org/10.1016/j.jclepro.2018.12.233

Vucko MJ, Magnusson M, Kinley RD, Villart C, Nys R (2017). The effects of processing on the in vitro anti methanogenic capacity and concentration of secondary metabolites of Asparagopsis taxiformis. J. Appl. Phycol., 29:1577–1586. https://doi.org/10.1007/s10811-016-1004-3

Zeller WE (2019). Activity, purification, and analysis of condensed tannins: Current state of affairs and future endeavors. Crop Sci., 59: 886-904. https://doi.org/10.2135/cropsci2018.05.0323