● Microbial fermentation in the rumen is a main source of methane emissions.
● Nutritional strategies can effectively mitigate methane emissions by manipulating biochemical reactions in the methanogenesis pathways.
● Mitigation practices must be evaluated in an integrated animal production system instead of as isolated components.
Within the agricultural sector, animal production contributes to 14.5% of global anthropogenic greenhouse gas emissions and produces around 37% of global CH4 emissions, mainly due to ruminal fermentation in ruminants. Over 90% of CH4 is synthesized by methanogens in the rumen during carbohydrate fermentation. According to different substrates, methanogenesis pathways can be divided into four categories: (1) hydrogenotrophic pathway; (2) acetoclastic pathway; (3) methyl dismutation pathway; and (4) methyl-reducing pathway. Based on the principle of biochemical reactions in the methanogenesis pathways, this paper reviews the latest publications on CH4 decreases in ruminants and described three nutritional strategies in terms of dietary nutrient manipulation (feeding management, feed composition, forage quality and lipids), microbial manipulation (ionophore, defaunation, methanogen inhibitors and probiotics), and chemical manipulation (nitrate, organic acids, plant secondary metabolites and phlorotannins, or halides in seaweeds). For each mitigation strategy, the review discusses effectiveness for decreasing CH4 emissions, application prescription, and feed safety based on results from in vitro and in vivo studies. This review summarizes different nutritional strategies to mitigate CH4 emissions and proposed comprehensive approaches for future feeding interventions and applications in the livestock industry.
C, Opio P, Gerber A, Mottet A, Falcucci G, Tempio M, Macleod T, Vellinga B, Henderson H Steinfeld . Greenhouse gas emissions from ruminant supply chains: a global life cycle assessment. Rome: Food and Agriculture Organization of the United Nations (FAO), 2013
2
P J, Gerber H, Steinfeld B, Henderson A, Mottet C, Opio J, Dijkman A, Falcucci G Tempio . Tackling climate change through livestock: a global assessment of emissions and mitigation opportunities. Rome: Food and Agriculture Organization of the United Nations (FAO), 2013
3
R, Mendonça R A, Müller D, Clow C, Verpoorter P, Raymond L J, Tranvik S Sobek . Organic carbon burial in global lakes and reservoirs. Nature Communications, 2017, 8(1): 1694 https://doi.org/10.1038/s41467-017-01789-6
pmid: 29162815
4
K A, Beauchemin E M, Ungerfeld R J, Eckard M Wang . Review: Fifty years of research on rumen methanogenesis: lessons learned and future challenges for mitigation. Animal, 2020, 14(S1): s2–s16 https://doi.org/10.1017/S1751731119003100
pmid: 32024560
5
Z, Liu K, Wang X, Nan M, Cai L, Yang B, Xiong Y Zhao . Synergistic effects of 3-nitrooxypropanol with fumarate in the regulation of propionate formation and methanogenesis in dairy cows in vitro. Applied and Environmental Microbiology, 2022, 88(6): e0190821
6
G, Grossi P, Goglio A, Vitali A G Williams . Livestock and climate change: impact of livestock on climate and mitigation strategies. Animal Frontiers, 2018, 9(1): 69–76 https://doi.org/10.1093/af/vfy034
pmid: 32071797
7
C J, Newbold la Fuente G, de A, Belanche E, Ramos-Morales N R McEwan . The role of ciliate protozoa in the rumen. Frontiers in Microbiology, 2015, 6: 1313 https://doi.org/10.3389/fmicb.2015.01313
pmid: 26635774
8
G, Henderson F, Cox S, Ganesh A, Jonker W, Young P H Janssen . Rumen microbial community composition varies with diet and host, but a core microbiome is found across a wide geographical range. Scientific Reports, 2015, 5(1): 14567 https://doi.org/10.1038/srep14567
pmid: 26449758
9
S, Kittelmann C S, Pinares-Patiño H, Seedorf M R, Kirk S, Ganesh J C, McEwan P H Janssen . Two different bacterial community types are linked with the low-methane emission trait in sheep. PLoS One, 2014, 9(7): e103171 https://doi.org/10.1371/journal.pone.0103171
pmid: 25078564
10
R, Danielsson J, Dicksved L, Sun H, Gonda B, Müller A, Schnürer J Bertilsson . Methane production in dairy cows correlates with rumen methanogenic and bacterial community structure. Frontiers in Microbiology, 2017, 8: 226 https://doi.org/10.3389/fmicb.2017.00226
pmid: 28261182
11
D, Pitta N, Indugu K, Narayan M Hennessy . Symposium review: understanding the role of the rumen microbiome in enteric methane mitigation and productivity in dairy cows. Journal of Dairy Science, 2022, 105(10): 8569–8585 https://doi.org/10.3168/jds.2021-21466
pmid: 35346473
12
R, Solomon T, Wein B, Levy S, Eshed R, Dror V, Reiss T, Zehavi O, Furman I, Mizrahi E Jami . Protozoa populations are ecosystem engineers that shape prokaryotic community structure and function of the rumen microbial ecosystem. ISME Journal, 2022, 16(4): 1187–1197 https://doi.org/10.1038/s41396-021-01170-y
pmid: 34887549
13
L Y, Liu G J, Xie J, Ding B F, Liu D F, Xing N Q, Ren Q Wang . Microbial methane emissions from the non-methanogenesis processes: a critical review. Science of the Total Environment, 2022, 806(Pt 4): 151362
14
Y, Li W, Jin Y, Cheng W Zhu . Effect of the associated methanogen Methanobrevibacter thaueri on the dynamic profile of end and intermediate metabolites of anaerobic fungus Piromyces sp. F1. Current Microbiology, 2016, 73(3): 434–441 https://doi.org/10.1007/s00284-016-1078-9
pmid: 27287262
15
Y F, Cheng J E, Edwards G G, Allison W Y, Zhu M K Theodorou . Diversity and activity of enriched ruminal cultures of anaerobic fungi and methanogens grown together on lignocellulose in consecutive batch culture. Bioresource Technology, 2009, 100(20): 4821–4828 https://doi.org/10.1016/j.biortech.2009.04.031
pmid: 19467591
16
A, Reisinger H, Clark A L, Cowie J, Emmet-Booth Fischer C, Gonzalez M, Herrero M, Howden S Leahy . How necessary and feasible are reductions of methane emissions from livestock to support stringent temperature goals. Philosophical Transactions A: Mathematical, Physical, and Engineering Sciences, 2021, 379(2210): 20200452 https://doi.org/10.1098/rsta.2020.0452
pmid: 34565223
17
S A, Huws C J, Creevey L B, Oyama I, Mizrahi S E, Denman M, Popova R, Muñoz-Tamayo E, Forano S M, Waters M, Hess I, Tapio H, Smidt S J, Krizsan D R, Yáñez-Ruiz A, Belanche L, Guan R J, Gruninger T A, McAllister C J, Newbold R, Roehe R J, Dewhurst T J, Snelling M, Watson G, Suen E H, Hart A H, Kingston-Smith N D, Scollan Prado R M, do E J, Pilau H C, Mantovani G T, Attwood J E, Edwards N R, McEwan S, Morrisson O L, Mayorga C, Elliott D P Morgavi . Addressing global ruminant agricultural challenges through understanding the rumen microbiome: past, present, and future. Frontiers in Microbiology, 2018, 9: 2161 https://doi.org/10.3389/fmicb.2018.02161
pmid: 30319557
18
A, Söllinger C, Schwab T, Weinmaier A, Loy A T, Tveit C, Schleper T Urich . Phylogenetic and genomic analysis of Methanomassiliicoccales in wetlands and animal intestinal tracts reveals clade-specific habitat preferences. FEMS Microbiology Ecology, 2016, 92(1): fiv149 https://doi.org/10.1093/femsec/fiv149
pmid: 26613748
19
Y, Li S C, Leahy J, Jeyanathan G, Henderson F, Cox E, Altermann W J, Kelly S C, Lambie P H, Janssen J, Rakonjac G T Attwood . The complete genome sequence of the methanogenic archaeon ISO4-H5 provides insights into the methylotrophic lifestyle of a ruminal representative of the Methanomassiliicoccales. Standards in Genomic Sciences, 2016, 11(1): 59 https://doi.org/10.1186/s40793-016-0183-5
pmid: 27602181
20
de Mesquita C P, Bueno D, Wu S G Tringe . Methyl-based methanogenesis: an ecological and genomic review. Microbiology and Molecular Biology Reviews, 2023, 87(1): e0002422 https://doi.org/10.1128/mmbr.00024-22
pmid: 36692297
21
E M Ungerfeld . Inhibition of rumen methanogenesis and ruminant productivity: a meta-analysis. Frontiers in Veterinary Science, 2018, 5: 113 https://doi.org/10.3389/fvets.2018.00113
pmid: 29971241
22
Y, Liu W B Whitman . Metabolic, phylogenetic, and ecological diversity of the methanogenic archaea. Annals of the New York Academy of Sciences, 2008, 1125(1): 171–189 https://doi.org/10.1196/annals.1419.019
pmid: 18378594
23
K, Lang J, Schuldes A, Klingl A, Poehlein R, Daniel A Brunea . New mode of energy metabolism in the seventh order of methanogens as revealed by comparative genome analysis of “Candidatus methanoplasma termitum”. Applied and Environmental Microbiology, 2015, 81(4): 1338–1352 https://doi.org/10.1128/AEM.03389-14
pmid: 25501486
24
K A, Beauchemin E M, Ungerfeld A L, Abdalla C, Alvarez C, Arndt P, Becquet C, Benchaar A, Berndt R M, Mauricio T A, McAllister W, Oyhantçabal S A, Salami L, Shalloo Y, Sun J, Tricarico A, Uwizeye Camillis C, De M, Bernoux T, Robinson E Kebreab . Invited review: Current enteric methane mitigation options. Journal of Dairy Science, 2022, 105(12): 9297–9326 https://doi.org/10.3168/jds.2022-22091
pmid: 36270879
25
M L, Galyean K E Hales . Feeding management strategies to mitigate methane and improve production efficiency in feedlot cattle. Animals, 2023, 13(4): 758 https://doi.org/10.3390/ani13040758
pmid: 36830545
26
J, Vargas E, Ungerfeld C, Muñoz N DiLorenzo . Feeding strategies to mitigate enteric methane emission from ruminants in grassland systems. Animals, 2022, 12(9): 1132 https://doi.org/10.3390/ani12091132
pmid: 35565559
27
K J, Hammond A K, Jones D J, Humphries L A, Crompton C K Reynolds . Effects of diet forage source and neutral detergent fiber content on milk production of dairy cattle and methane emissions determined using GreenFeed and respiration chamber techniques. Journal of Dairy Science, 2016, 99(10): 7904–7917 https://doi.org/10.3168/jds.2015-10759
pmid: 27522422
28
G, Gislon S, Colombini G, Borreani G M, Crovetto A, Sandrucci G, Galassi E, Tabacco L Rapetti . Milk production, methane emissions, nitrogen, and energy balance of cows fed diets based on different forage systems. Journal of Dairy Science, 2020, 103(9): 8048–8061 https://doi.org/10.3168/jds.2019-18134
pmid: 32622607
29
C, Martin A, Ferlay P, Mosoni Y, Rochette Y, Chilliard M Doreau . Increasing linseed supply in dairy cow diets based on hay or corn silage: effect on enteric methane emission, rumen microbial fermentation, and digestion. Journal of Dairy Science, 2016, 99(5): 3445–3456 https://doi.org/10.3168/jds.2015-10110
pmid: 26947299
30
A K, Patra Z Yu . Effects of essential oils on methane production and fermentation by, and abundance and diversity of, rumen microbial populations. Applied and Environmental Microbiology, 2012, 78(12): 4271–4280 https://doi.org/10.1128/AEM.00309-12
pmid: 22492451
31
X M, Zhang R F, Medrano M, Wang K A, Beauchemin Z Y, Ma R, Wang J N, Wen B A, Lukuyu Z L, Tan J H He . Corn oil supplementation enhances hydrogen use for biohydrogenation, inhibits methanogenesis, and alters fermentation pathways and the microbial community in the rumen of goats. Journal of Animal Science, 2019, 97(12): 4999–5008 https://doi.org/10.1093/jas/skz352
pmid: 31740932
32
J V, Judy G C, Bachman T M, Brown-Brandl S C, Fernando K E, Hales P S, Miller R R, Stowell P J Kononoff . Reducing methane production with corn oil and calcium sulfate: Responses on whole-animal energy and nitrogen balance in dairy cattle. Journal of Dairy Science, 2019, 102(3): 2054–2067 https://doi.org/10.3168/jds.2018-14567
pmid: 30612805
33
W L, Crossland L O, Tedeschi T R, Callaway M D, Miller W B, Smith M Cravey . Effects of rotating antibiotic and ionophore feed additives on volatile fatty acid production, potential for methane production, and microbial populations of steers consuming a moderate-forage diet. Journal of Animal Science, 2017, 95(10): 4554–4567 https://doi.org/10.2527/jas2017.1665
pmid: 29108045
34
E A, Melchior K E, Hales A K, Lindholm-Perry H C, Freetly J E, Wells C N, Hemphill T A, Wickersham J E, Sawyer P R Myer . The effects of feeding monensin on rumen microbial communities and methanogenesis in bred heifers fed in a drylot. Livestock Science, 2018, 212: 131–136 https://doi.org/10.1016/j.livsci.2018.03.019
35
J A D R N, Appuhamy A B, Strathe S, Jayasundara C, Wagner-Riddle J, Dijkstra J, France E Kebreab . Anti-methanogenic effects of monensin in dairy and beef cattle: a meta-analysis. Journal of Dairy Science, 2013, 96(8): 5161–5173 https://doi.org/10.3168/jds.2012-5923
pmid: 23769353
36
C Benchaar . Diet supplementation with cinnamon oil, cinnamaldehyde, or monensin does not reduce enteric methane production of dairy cows. Animal, 2016, 10(3): 418–425 https://doi.org/10.1017/S175173111500230X
pmid: 26888487
37
R N S, Torres J R, Paschoaloto J M B, Ezequiel Silva D A V, da M T C Almeida . Meta-analysis of the effects of essential oil as an alternative to monensin in diets for beef cattle. Veterinary Journal, 2021, 272: 105659 https://doi.org/10.1016/j.tvjl.2021.105659
pmid: 33941330
38
X, Dai K F, Kalscheur P, Huhtanen A P Faciola . Effects of ruminal protozoa on methane emissions in ruminants—A meta-analysis. Journal of Dairy Science, 2022, 105(9): 7482–7491 https://doi.org/10.3168/jds.2021-21139
pmid: 35931473
39
L, Abecia P G, Toral A I, Martín-García G, Martínez N W, Tomkins E, Molina-Alcaide C J, Newbold D R Yáñez-Ruiz . Effect of bromochloromethane on methane emission, rumen fermentation pattern, milk yield, and fatty acid profile in lactating dairy goats. Journal of Dairy Science, 2012, 95(4): 2027–2036 https://doi.org/10.3168/jds.2011-4831
pmid: 22459848
40
K D, Allen R H White . Chapter seventeen—Identification of the radical SAM enzymes involved in the biosynthesis of methanopterin and coenzyme F420 in methanogens. In: Bandarian V, ed. Methods in Enzymology. Academic Press, 2018, 606: 461–483
41
L Jr, Kung A O, Hession J P Bracht . Inhibition of sulfate reduction to sulfide by 9,10-anthraquinone in in vitro ruminal fermentations. Journal of Dairy Science, 1998, 81(8): 2251–2256 https://doi.org/10.3168/jds.S0022-0302(98)75804-7
pmid: 9749391
42
Casañas M A, Aguinaga N, Rangkasenee N, Krattenmacher G, Thaller C C, Metges B Kuhla . Methyl-coenzyme M reductase A as an indicator to estimate methane production from dairy cows. Journal of Dairy Science, 2015, 98(6): 4074–4083 https://doi.org/10.3168/jds.2015-9310
pmid: 25841964
43
J, Dijkstra A, Bannink J, France E, Kebreab Gastelen S van . Short communication: Antimethanogenic effects of 3-nitrooxypropanol depend on supplementation dose, dietary fiber content, and cattle type. Journal of Dairy Science, 2018, 101(10): 9041–9047 https://doi.org/10.3168/jds.2018-14456
pmid: 30055923
44
A, Romero-Perez E K, Okine S M, McGinn L L, Guan M, Oba S M, Duval M, Kindermann K A Beauchemin . The potential of 3-nitrooxypropanol to lower enteric methane emissions from beef cattle. Journal of Animal Science, 2014, 92(10): 4682–4693 https://doi.org/10.2527/jas.2014-7573
pmid: 25184838
45
A, Melgar C F A, Lage K, Nedelkov S E, Räisänen H, Stefenoni M E, Fetter X, Chen J, Oh S, Duval M, Kindermann N D, Walker A N Hristov . Enteric methane emission, milk production, and composition of dairy cows fed 3-nitrooxypropanol. Journal of Dairy Science, 2021, 104(1): 357–366 https://doi.org/10.3168/jds.2020-18908
pmid: 33131815
46
A, Jayanegara K A, Sarwono M, Kondo H, Matsui M, Ridla E B, Laconi Nahrowi. Use of 3-nitrooxypropanol as feed additive for mitigating enteric methane emissions from ruminants: a meta-analysis. Italian Journal of Animal Science, 2018, 17(3): 650–656 https://doi.org/10.1080/1828051X.2017.1404945
47
G, Martinez-Fernandez S, Duval M, Kindermann H J, Schirra S E, Denman C S McSweeney . 3-NOP vs. halogenated compound: methane production, ruminal fermentation and microbial community response in forage fed cattle. Frontiers in Microbiology, 2018, 9: 1582 https://doi.org/10.3389/fmicb.2018.01582
pmid: 30131771
48
M E, Uddin J M, Tricarico E Kebreab . Impact of nitrate and 3-nitrooxypropanol on the carbon footprints of milk from cattle produced in confined-feeding systems across regions in the United States: a life cycle analysis. Journal of Dairy Science, 2022, 105(6): 5074–5083 https://doi.org/10.3168/jds.2021-20988
pmid: 35346477
49
B, Darabighane A Z M, Salem Aghjehgheshlagh F, Mirzaei A, Mahdavi A, Zarei M M M Y, Elghandour S López . Environmental efficiency of Saccharomyces cerevisiae on methane production in dairy and beef cattle via a meta-analysis. Environmental Science and Pollution Research International, 2019, 26(4): 3651–3658 https://doi.org/10.1007/s11356-018-3878-x
pmid: 30535735
50
J, Oh M, Harper A, Melgar D M P, Compart A N Hristov . Effects of Saccharomyces cerevisiae-based direct-fed microbial and exogenous enzyme products on enteric methane emission and productivity in lactating dairy cows. Journal of Dairy Science, 2019, 102(7): 6065–6075 https://doi.org/10.3168/jds.2018-15753
pmid: 31030921
51
A, Hassan H, Gado U Y, Anele M A M, Berasain A Z M Salem . Influence of dietary probiotic inclusion on growth performance, nutrient utilization, ruminal fermentation activities and methane production in growing lambs. Animal Biotechnology, 2020, 31(4): 365–372 https://doi.org/10.1080/10495398.2019.1604380
pmid: 31006376
52
C, Philippeau A, Lettat C, Martin M, Silberberg D P, Morgavi A, Ferlay C, Berger P Nozière . Effects of bacterial direct-fed microbials on ruminal characteristics, methane emission, and milk fatty acid composition in cows fed high- or low-starch diets. Journal of Dairy Science, 2017, 100(4): 2637–2650 https://doi.org/10.3168/jds.2016-11663
pmid: 28161181
53
M L, Villar R S, Hegarty J V, Nolan I R, Godwin M Mcphee . The effect of dietary nitrate and canola oil alone or in combination on fermentation, digesta kinetics and methane emissions from cattle. Animal Feed Science and Technology, 2020, 259: 114294 https://doi.org/10.1016/j.anifeedsci.2019.114294
54
H, Wu Q, Meng Z Yu . Effect of pH buffering capacity and sources of dietary sulfur on rumen fermentation, sulfide production, methane production, sulfate reducing bacteria, and total Archaea in in vitro rumen cultures. Bioresource Technology, 2015, 186: 25–33 https://doi.org/10.1016/j.biortech.2015.02.110
pmid: 25797103
55
S S, Paul S M, Deb D Singh . Isolation and characterization of novel sulphate-reducing Fusobacterium sp and their effects on in vitro methane emission and digestion of wheat straw by rumen fluid from Indian riverine buffaloes. Animal Feed Science and Technology, 2011, 166−167: 132−140
56
C, Lee R C, Araujo K M, Koenig K A Beauchemin . Effects of encapsulated nitrate on growth performance, nitrate toxicity, and enteric methane emissions in beef steers: backgrounding phase. Journal of Animal Science, 2017, 95(8): 3700–3711
pmid: 28805908
57
R A, Meller B A, Wenner J, Ashworth A M, Gehman J, Lakritz J L Firkins . Potential roles of nitrate and live yeast culture in suppressing methane emission and influencing ruminal fermentation, digestibility, and milk production in lactating Jersey cows. Journal of Dairy Science, 2019, 102(7): 6144–6156 https://doi.org/10.3168/jds.2018-16008
pmid: 31030922
58
L R, Rebelo I C, Luna J D, Messana R C, Araujo T A, Simioni Y T, Granja-Salcedo E S, Vito C, Lee I A M A, Teixeira J A, Rooke T T Berchielli . Effect of replacing soybean meal with urea or encapsulated nitrate with or without elemental sulfur on nitrogen digestion and methane emissions in feedlot cattle. Animal Feed Science and Technology, 2019, 257: 114293 https://doi.org/10.1016/j.anifeedsci.2019.114293
59
A, Ortiz-Chura J, Gere G, Marcoppido G, Depetris S, Cravero C, Faverín C, Pinares-Patiño A, Cataldi M E Cerón-Cucchi . Dynamics of the ruminal microbial ecosystem, and inhibition of methanogenesis and propiogenesis in response to nitrate feeding to Holstein calves. Animal Nutrition, 2021, 7(4): 1205–1218 https://doi.org/10.1016/j.aninu.2021.07.005
pmid: 34754962
60
J L, Vanegas J, González M R, Alvir M D Carro . Influence of malic acid-heat treatment for protecting sunflower protein against ruminal degradation on in vitro methane production: a comparison with the use of malic acid as an additive. Animal Feed Science and Technology, 2017, 228: 123–131 https://doi.org/10.1016/j.anifeedsci.2017.04.015
61
R J, Wallace T A, Wood A, Rowe J, Price D R, Yanez S P, Williams C J Newbold . Encapsulated fumaric acid as a means of decreasing ruminal methane emissions. International Congress Series, 2006, 1293: 148–151 https://doi.org/10.1016/j.ics.2006.02.018
62
P A, Foley D A, Kenny D K, Lovett J J, Callan T M, Boland F P O’Mara . Effect of DL-malic acid supplementation on feed intake, methane emissions, and performance of lactating dairy cows at pasture. Journal of Dairy Science, 2009, 92(7): 3258–3264 https://doi.org/10.3168/jds.2008-1633
pmid: 19528602
63
G, Cobellis M, Trabalza-Marinucci Z Yu . Critical evaluation of essential oils as rumen modifiers in ruminant nutrition: a review. Science of the Total Environment, 2016, 545–546: 556–568
64
M, Rira D P, Morgavi M, Popova G, Maxin M Doreau . Microbial colonisation of tannin-rich tropical plants: interplay between degradability, methane production and tannin disappearance in the rumen. Animal, 2022, 16(8): 100589 https://doi.org/10.1016/j.animal.2022.100589
pmid: 35839617
65
R G, Christensen J S, Eun S Y, Yang B R, Min J W Macadam . In vitro effects of birdsfoot trefoil (Lotus corniculatus L.) pasture on ruminal fermentation, microbial population, and methane production. Professional Animal Scientist, 2017, 33(4): 451–460 https://doi.org/10.15232/pas.2016-01558
66
B R, Min S, Solaiman H M, Waldrip D, Parker R W, Todd D Brauer . Dietary mitigation of enteric methane emissions from ruminants: a review of plant tannin mitigation options. Animal Nutrition, 2020, 6(3): 231–246 https://doi.org/10.1016/j.aninu.2020.05.002
pmid: 33005757
67
G, Animut R, Puchala A L, Goetsch A K, Patra T, Sahlu V H, Varel J Wells . Methane emission by goats consuming diets with different levels of condensed tannins from lespedeza. Animal Feed Science and Technology, 2008, 144(3−4): 212−227
68
W K, Krueger H, Gutierrez-Bañuelos G E, Carstens B R, Min W E, Pinchak R R, Gomez R C, Anderson N A, Krueger T D A Forbes . Effects of dietary tannin source on performance, feed efficiency, ruminal fermentation, and carcass and non-carcass traits in steers fed a high-grain diet. Animal Feed Science and Technology, 2010, 159(1−2): 1−9
69
B R, Min K, Hernandez W E, Pinchak R C, Anderson J E, Miller E Valencia . Effects of plant tannin extracts supplementation on animal performance and gastrointestinal parasites infestation in steers grazing winter wheat. Open Journal of Animal Sciences, 2015, 5(3): 343–350 https://doi.org/10.4236/ojas.2015.53038
70
A, Jayanegara G, Goel H P S, Makkar K Becker . Divergence between purified hydrolysable and condensed tannin effects on methane emission, rumen fermentation and microbial population in vitro. Animal Feed Science and Technology, 2015, 209: 60−68
71
L, He N, Chen H, Lv C, Wang W, Zhou X, Chen Q Zhang . Gallic acid influencing fermentation quality, nitrogen distribution and bacterial community of high-moisture mulberry leaves and stylo silage. Bioresource Technology, 2020, 295: 122255 https://doi.org/10.1016/j.biortech.2019.122255
pmid: 31639626
72
M, Rira D P, Morgavi L, Genestoux S, Djibiri I, Sekhri M Doreau . Methanogenic potential of tropical feeds rich in hydrolyzable tannins1,2. Journal of Animal Science, 2019, 97(7): 2700–2710 https://doi.org/10.1093/jas/skz199
pmid: 31192352
73
T, Ampapon K, Phesatcha M Wanapat . Effects of phytonutrients on ruminal fermentation, digestibility, and microorganisms in swamp buffaloes. Animals, 2019, 9(9): 671 https://doi.org/10.3390/ani9090671
pmid: 31514374
74
T, Ampapon M Wanapat . Dietary rambutan peel powder as a rumen modifier in beef cattle. Asian-Australasian Journal of Animal Sciences, 2020, 33(5): 763–769 https://doi.org/10.5713/ajas.19.0342
pmid: 31480168
75
M, Matra P, Totakul M Wanapat . Utilization of dragon fruit waste by-products and non-protein nitrogen source: effects on in vitro rumen fermentation, nutrients degradability and methane production. Livestock Science, 2021, 243: 104386 https://doi.org/10.1016/j.livsci.2020.104386
76
M, Wanapat B, Viennasay M, Matra P, Totakul B, Phesatcha T, Ampapon S Wanapat . Supplementation of fruit peel pellet containing phytonutrients to manipulate rumen pH, fermentation efficiency, nutrient digestibility and microbial protein synthesis. Journal of the Science of Food and Agriculture, 2021, 101(11): 4543–4550 https://doi.org/10.1002/jsfa.11096
pmid: 33452814
77
P R, Lima T, Apdini A S, Freire A S, Santana L M L, Moura J C S, Nascimento R T S, Rodrigues J, Dijkstra Neto A F, Garcez M A A, Queiroz D R Menezes . Dietary supplementation with tannin and soybean oil on intake, digestibility, feeding behavior, ruminal protozoa and methane emission in sheep. Animal Feed Science and Technology, 2019, 249: 10–17 https://doi.org/10.1016/j.anifeedsci.2019.01.017
78
C A, Ramirez-Restrepo C, Tan C J, O’neill N, Lopez-Villalobos J, Padmanabha J, Wang C S Mcsweeney . Methane production, fermentation characteristics, and microbial profiles in the rumen of tropical cattle fed tea seed saponin supplementation. Animal Feed Science and Technology, 2016, 216: 58–67 https://doi.org/10.1016/j.anifeedsci.2016.03.005
79
J, Guyader M, Eugène M, Doreau D P, Morgavi C, Gérard C Martin . Tea saponin reduced methanogenesis in vitro but increased methane yield in lactating dairy cows. Journal of Dairy Science, 2017, 100(3): 1845–1855 https://doi.org/10.3168/jds.2016-11644
pmid: 28109588
80
B R, Min D, Parker D, Brauer H, Waldrip C, Lockard K, Hales A, Akbay S Augyte . The role of seaweed as a potential dietary supplementation for enteric methane mitigation in ruminants: challenges and opportunities. Animal Nutrition, 2021, 7(4): 1371–1387 https://doi.org/10.1016/j.aninu.2021.10.003
pmid: 34786510
81
Y, Wang Z, Xu S J, Bach T A Mcallister . Effects of phlorotannins from Ascophyllum nodosum (brown seaweed) on in vitro ruminal digestion of mixed forage or barley grain. Animal Feed Science and Technology, 2008, 145(1−4): 375−395
82
B M, Roque M, Venegas R D, Kinley Nys R, de T L, Duarte X, Yang E Kebreab . Red seaweed (Asparagopsis taxiformis) supplementation reduces enteric methane by over 80 percent in beef steers. PLoS One, 2021, 16(3): e0247820 https://doi.org/10.1371/journal.pone.0247820
pmid: 33730064
83
X, Li H C, Norman R D, Kinley M, Laurence M, Wilmot H, Bender Nys R, De N Tomkins . Asparagopsis taxiformis decreases enteric methane production from sheep. Animal Production Science, 2018, 58(4): 681–688 https://doi.org/10.1071/AN15883