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doi: 10.15389/agrobiology.2024.2.221eng

UDC: 636.2/.3:636.085.22

Acknowledgements:
The study was carried out within the framework of the state task FGGN-2022-0009.

 

THE EFFECT OF DIFFERENT CLASSES OF TANNINS ON METHANOGENESIS IN RUMINANTS (review)

N.S. Kolesnik , N.V. Bogolyubova, A.A. Zelenchenkova

Ernst Federal Research Center for Animal Husbandry, 60, pos. Dubrovitsy, Podolsk District, Moscow Province, 142132 Russia, e-mail kominisiko@mail.ru (✉ corresponding author), 652202@mail.ru, aly4383@mail.ru

ORCID:
Kolesnik N.S. orcid.org/0000-0002-4267-5300
Zelenchenkova A.A. orcid.org/0000-0001-8862-3648
Bogolyubova N.V. orcid org/0000-0002-0520-7022

Final revision received September 07, 2023
Accepted October 29, 2023

The emission of greenhouse gases by ruminants is becoming an urgent environmental problem. Methane has the highest global warming potential among greenhouse gases (R.A. Muller et al., 2017). Reducing gastrointestinal CH4 emissions will help improve energy efficiency and reduce the environmental burden from agriculture (I.V. Petrunina et al., 2022). There are several strategies to reduce greenhouse gas emissions from ruminants, in particular, nutrition management and the use of various feed additives (N.V. Bogolyubova et al., 2022). Various fat additives are also used to reduce methane emissions. Dietary unsaturated fatty acids (FFAs) have a detrimental effect on methanogens and protozoa and reduces the acetate/propionate ratio in the rumen, resulting in reduced methane production (J.O. Zeitz et al., 2013). Another promising strategy to reduce methane emissions is the use of secondary plant metabolites as feed additives. In particular, these are tannins which have anti-methanogenic potential, pronounced antioxidant, antimicrobial properties, and can form complexes with proteins and some trace elements due to the presence of a large amount of phenolic hydroxyl groups (A.I. Roca-Fernández et al., 2020; P.R. Lima et al., 2019). These are high molecular weight polyphenolic compounds of two groups, the condensed and hydrolysable tannins (A.K. Patra et al., 2010). Their biological activity largely depends on the chemical structure and dosage. Hydrolysable tannins at high concentrations have a toxic effect, unlike condensed tannins. Mechanisms of tannins’ action are not fully understood. One hypothesis is that tannins act directly on methanogens in the rumen, changing the membrane permeability of some rumen microorganisms and inhibiting their enzymatic activity (M. Caetano et al., 2019). Another hypothesis is that indirect inhibition occurs due to a decrease in the availability of nutrients for rumen microorganisms, which subsequently reduces the digestibility of the substrate and indirectly inhibits rumen microbial populations (H.D. Naumann et al., 2017). A third hypothesis for how tannins, namely condensed tannins, inhibit CH4 production is that they act as a proton scavenger (H.D. Naumann et al., 2017). To date, a lot of work is underway to study the effect of various classes of tannins on the cicatricial microbiota and methanogenesis. Numerous in vitro and in vivo studies show that the inclusion of tannins directly from plants or as plant extracts in the diet of ruminants leads to a decrease in CH4 emission (F. Hassanat et al., 2013, H.M. El-Zaiat et al., 2020). Some studies also evaluate the effect of a mixture of condensed and hydrolysable tannins on rumen fermentation (C.J. Marshall et al., 2022).

Keywords: hydrolysable tannins, condensed tannins, methanogenesis, rumen microbiome, ruminants.

 

REFERENCES

  1. Cardoso-Gutierrez E., Aranda-Aguirre E., Robles-Jimenez L.E., Castelán-Ortega O.A., Chay-Canul A.J., Foggi G., Angeles-Hernandez J.C., Vargas-Bello-Pérez E., González-Ronquillo M. Effect of tannins from tropical plants on methane production from ruminants: a systematic review. Veterinary and Animal Science, 2021, 14: 100214 CrossRef
  2. Cardona-Iglesias J.L., Mahecha-Ledesma L., Angulo-Arizala J. Arbustivas forrajeras y ácidos grasos: estrategias para disminuir la producción de metano entérico en bovinos. Agronomía Mesoamericana, 2017, 28(1): 273-288 CrossRef
  3. Eugène M., Klumpp K., Sauvant D. Methane mitigating options with forages fed to ruminants. Grass and Forage Science, 2021, 76(2): 196-204 CrossRef
  4. Audsley E., Wilkinson M. What is the potential for reducing national greenhouse gas emissions from crop and livestock production systems? Journal of Cleaner Production, 2014, 73: 263-268 CrossRef
  5. Slade E.M., Riutta T., Roslin T., Tuomisto H.L. The role of dung beetles in reducing greenhouse gas emissions from cattle farming. Scientific Reports, 2016, 6(1): 1-9 CrossRef
  6. Gerber P.J., Hristov A.N., Henderson B., Makkar H., Oh J., Lee C., Meinen R., Montes F., Ott T., Firkins J., Rotz A., Dell C., Adesogan A.T., Yang W. Z., Tricarico J.M., Kebreab E., Waghorn G., Dijkstra J., Oosting S. Technical options for the mitigation of direct methane and nitrous oxide emissions from livestock: a review. Animal, 2013, 7(s2): 220-234 CrossRef
  7. Vargas J., Ungerfeld E., Muñoz C., DiLorenzo N. Feeding strategies to mitigate enteric methane emission from ruminants in grassland systems. Animals, 2022, 12(9): 1132 CrossRef
  8. Focant M., Froidmont E., Archambeau Q., Van Q.D., Larondelle Y. The effect of oak tannin (Quercus robur) and hops (Humulus lupulus) on dietary nitrogen efficiency, methane emission, and milk fatty acid composition of dairy cows fed a low-protein diet including linseed. Journal of Dairy Science, 2019, 102(2): 1144-1159 CrossRef
  9. Eckard R.J., Grainger C., de Klein C.A.M. Options for the abatement of methane and nitrous oxide from ruminant production: a review. Livestock Science, 2010, 130(1-3): 47-56 CrossRef
  10. Dijkstra J., Oenema O., Van Groenigen J.W., Spek J.W., van Vuuren A.M., Bannink A. Diet effects on urine composition of cattle and N2O emissions. Animal, 2013, 7(s2): 292-302 CrossRef
  11. Fedorov Yu.A., Sukhorukov V.V., Trubnik R.G. Antropogennaya transformatsiya prirodnoy sredy, 2021, 7(1): 6-34 CrossRef (in Russ.).
  12. Muller R.A., Muller E.A. Fugitive methane and the role of atmospheric half-life. Geoinformatics & Geostatistics: An Overview, 2017, 5(3): 1-7 CrossRef
  13. Ugbogu E.A., Elghandour M.M.M.Y., Ikpeazu V.O., Buendía G.R., Molina O.M., Arunsi U.O., Okezie E., Salem A.Z.M. The potential impacts of dietary plant natural products on the sustainable mitigation of methane emission from livestock farming. Journal of Cleaner Production, 2019, 213: 915-925 CrossRef
  14. Eliseev A.V. Fundamental’naya i prikladnaya klimatologiya, 2018, 1: 52-70 CrossRef (in Russ.).
  15. Rira M., Chentli A., Boufenera S., Bousseboua H. Effects of plants containing secondary metabolites on ruminal methanogenesis of sheep in vitro. Energy Procedia, 2015, 74: 15-24 CrossRef
  16. Dong L.F., Ferris C.P., McDowell D.A., Yan T. Effects of diet forage proportion on maintenance energy requirement and the efficiency of metabolizable energy use for lactation by lactating dairy cows. Journal of Dairy Science, 2015, 98(12): 8846-8855 CrossRef
  17. Hristov A.N., Oh J., Giallongo F., Frederick T.W., Harper M.T., Weeks H.L., Branco A.F., Moate P.J., Deighton M.H., Williams S.R.O., Kindermann M., Duval S. An inhibitor persistently decreased enteric methane emission from dairy cows with no negative effect on milk production. Proceedings of the National Academy of Sciences, 2015, 112(34): 10663-10668 CrossRef
  18. Bhatta R., Uyeno Y., Tajima K., Takenaka A., Yabumoto Y., Nonaka I., Enishi O., Kurihara M. Difference in the nature of tannins on in vitro ruminal methane and volatile fatty acid production and on methanogenic archaea and protozoal populations. Journal of Dairy Science, 2009, 92(11): 5512-5522 CrossRef
  19. Dong L., Li B., Diao Q. Effects of dietary forage proportion on feed intake, growth performance, nutrient digestibility, and enteric methane emissions of Holstein heifers at various growth stages. Animals, 2019, 9(10): 725 CrossRef
  20. Petrunina I.V., Gorbunova N.A. Pishchevye sistemy, 2022, 5(3): 202-211 CrossRef (in Russ.).
  21. Henderson G., Cox F., Ganesh S., Jonker A., Young W., Janssen P.H. 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 CrossRef
  22. Henderson G., Cook G.M., Ronimus R.S. Enzyme- and gene-based approaches for developing methanogen-specific compounds to control ruminant methane emissions: a review. Animal Production Science, 2016, 58(6): 1017-1026 CrossRef
  23. Seshadri R., Leahy S.C., Attwood G.T., Teh K.H., Lambie S.C., Cookson A.L, Eloe-Fadrosh E.A., Pavlopoulos G.A., Hadjithomas M., Varghese N.J., Paez-Espino D., Hungate1000 project collaborators, Perry R., Henderson G., Creevey C.J., Terrapon N., Lapebie P., Drula E., Lombard V., Rubin E., Kyrpides N.C., Henrissat B., Woyke T., Ivanova N.N., Kelly W.J. Cultivation and sequencing of rumen microbiome members from the Hungate1000 Collection. Nature biotechnology, 2018, 36(4): 359-367 CrossRef
  24. Ungerfeld E.M. Metabolic hydrogen flows in rumen fermentation: principles and possibilities of interventions. Frontiers in Microbiology, 2020, 11: 589 CrossRef
  25. Morgavi D.P., Forano E., Martin C., Newbold C.J. Microbial ecosystem and methanogenesis in ruminants. Animal, 2010, 4(7): 1024-1036 CrossRef
  26. Beauchemin K.A., Ungerfeld E.M., Eckard R.J., Wang M. Review: Fifty years of research on rumen methanogenesis: Lessons learned and future challenges for mitigation. Animal, 2020, 14(S1): s2-s16 CrossRef
  27. Eckard R.J., Clark H. Potential solutions to the major greenhouse-gas issues facing Australasian dairy farming. Animal Production Science, 2018, 60(1): 10-16 CrossRef
  28. Arndt C., Hristov A.N., Price W.J., McClelland S.C., Pelaez A.M., Cueva S.F., Dijkstra J., Bannink A., Bayat A.R., Crompton L.A., Eugène M.A., Enahoro D., Kebreab E., Kreuzer M., McGee M., Martin C., Newbold C.J., Reynolds C.K., Schwarm A., Shingfield K.J., Veneman J.B., Yáñez-Ruiz D.R., Yu Z. Full adoption of the most effective strategies to mitigate methane emissions by ruminants can help meet the 1.5 C target by 2030 but not 2050. Proceedings of the National Academy of Sciences, 2022, 119(20): e2111294119 CrossRef
  29. Hristov A.N., Oh J., Firkins J.L., Dijkstra J., Kebreab E., Waghorn G., Makkar H.P.S., Adesogan A.T., Yang W., Lee C., Gerber P.J., Henderson B., Tricarico J.M. Special topics—Mitigation of methane and nitrous oxide emissions from animal operations: I. A review of enteric methane mitigation options. Journal of Animal Science, 2013, 91(11): 5045-5069 CrossRef
  30. Bogolyubova N.V., Zelenchenkova A.A., Kolesnik N.S., Lahonin P.D. Rumen methane production and its reduction using nutritional factors (review). Sel'skokhozyaistvennaya biologiya [Agricultural Biology], 2022, 57(6): 1025-1054 CrossRef
  31. Knapp J.R., Laur G.L., Vadas P.A., Weiss W.P., Tricarico J.M. Invited review: Enteric methane in dairy cattle production: quantifying the opportunities and impact of reducing emissions. Journal of Dairy Science, 2014, 97(6): 3231-3261 CrossRef
  32. Almeida A.K., Hegarty R.S., Cowie A. Meta-analysis quantifying the potential of dietary additives and rumen modifiers for methane mitigation in ruminant production systems. Animal Nutrition, 2021, 7(4): 1219-1230 CrossRef
  33. Chow J.M., Van Kessel J.A.S., Russell J.B. Binding of radiolabeled monensin and lasalocid to ruminal microorganisms and feed. Journal of Animal Science, 1994, 72(6): 1630-1635 CrossRef
  34. Grainger C., Williams R., Eckard R.J., Hannah M.C. A high dose of monensin does not reduce methane emissions of dairy cows offered pasture supplemented with grain. Journal of Dairy Science, 2010, 93(11): 5300-5308 CrossRef
  35. Benchaar C. Diet supplementation with cinnamon oil, cinnamaldehyde, or monensin does not reduce enteric methane production of dairy cows. Animal, 2016, 10(3): 418-425 CrossRef
  36. da Silva Marques R., Cooke R.F. Effects of ionophores on ruminal function of beef cattle. Animals, 2021, 11(10): 2871 CrossRef
  37. Jouany J.-P., Morgavi D.P. Use of ‘natural’products as alternatives to antibiotic feed additives in ruminant production. Animal, 2007, 1(10): 1443-1466 CrossRef
  38. Witzig M., Zeder M., Rodehutscord M. Effect of the ionophore monensin and tannin extracts supplemented to grass silage on populations of ruminal cellulolytics and methanogens in vitro. Anaerobe, 2018, 50: 44-54 CrossRef
  39. Mao H.-L., Wang J.-K., Zhou Y.-Y., Liu J.-X. Effects of addition of tea saponins and soybean oil on methane production, fermentation and microbial population in the rumen of growing lambs. Livestock Science, 2010, 129(1-3): 56-62 CrossRef
  40. Zeitz J.O., Bucher S., Zhou X., Meile L., Kreuzer M., Soliva C.R. Inhhibitory effects of saturated fatty acids on methane production by methanogenic Archaea. Journal of Animal and Feed Sciences, 2013, 22(1): 44-49 CrossRef
  41. Guyader J., Eugène M., Doreau M., Morgavi D.P., Gérard C., Loncke C., Martin C. Nitrate but not tea saponin feed additives decreased enteric methane emissions in nonlactating cows. Journal of Animal Science, 2015, 93(11): 5367-5377 CrossRef
  42. Guyader J., Eugène M., Meunier B., Doreau M., Morgavi D.P., Silberberg M., Rochette Y., Gerard C., Loncke C., Martin C. Additive methane-mitigating effect between linseed oil and nitrate fed to cattle. Journal of Animal Science, 2015, 93(7): 3564-3577 CrossRef
  43. Ungerfeld E.M. Shifts in metabolic hydrogen sinks in the methanogenesis-inhibited ruminal fermentation: a meta-analysis. Frontiers in Microbiology, 2015, 6: 37 CrossRef
  44. Grainger C., Beauchemin K.A. Can enteric methane emissions from ruminants be lowered without lowering their production? Animal Feed Science and Technology, 2011, 166-167: 308-320 CrossRef
  45. Martin C., Morgavi D.P., Doreau M. Methane mitigation in ruminants: from microbe to the farm scale. Animal, 2010, 4(3): 351-365 CrossRef
  46. Doreau M., Bauchart D., Chilliard Y. Enhancing fatty acid composition of milk and meat through animal feeding. Animal Production Science, 2010, 51(1): 19-29 CrossRef
  47. Livingstone K.M., Humphries D.J., Kirton P., Kliem K.E., Givens D.I., Reynolds C.K. Effects of forage type and extruded linseed supplementation on methane production and milk fatty acid composition of lactating dairy cows. Journal of Dairy Science, 2015, 98(6): 4000-4011 CrossRef
  48. Martin C., Ferlay A., Mosoni P., Rochette Y., Chilliard Y., Doreau M. 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 CrossRef
  49. Fiorentini G., Carvalho I.P.C., Messana J.D., Castagnino P.S., Berndt A., Canesin R.C., Frighetto R.T.S., Berchielli T.T. Effect of lipid sources with different fatty acid profiles on the intake, performance, and methane emissions of feedlot Nellore steers. Journal of Animal Science, 2014, 92(4): 1613-1620 CrossRef
  50. Carvalho I.P.C., Fiorentini G., Berndt A., Castagnino P.D.S., Messana J.D., Frighetto R.T.S., Reis R.A., Berchielli T.T. Performance and methane emissions of Nellore steers grazing tropical pasture supplemented with lipid sources. Revista Brasileira de Zootecnia, 2016, 45(12): 760-767 CrossRef
  51. Guyader J., Doreau M., Morgavi D.P., Gérard C., Loncke C., Martin C. Long-term effect of linseed plus nitrate fed to dairy cows on enteric methane emission and nitrate and nitrite residuals in milk. Animal, 2016, 10(7): 1173-1181 CrossRef
  52. Jose Neto A., Messana J.D., Ribeiro A.F., Vito E.S., Rossi L.G., Berchielli T.T. Effect of starch-based supplementation level combined with oil on intake, performance, and methane emissions of growing Nellore bulls on pasture. Journal of Animal Science, 2015, 93(5): 2275-2284 CrossRef
  53. Jose Neto A., Messana J.D., Rossi L.G., Carvalho I.P.C., Berchielli T.T. Methane emissions from Nellore bulls on pasture fed two levels of starch-based supplement with or without a source of oil. Animal Production Science, 2018, 59(4): 654-663 CrossRef
  54. Silva R.A., Fiorentini G., Messana J.D., Lage J.F., Castagnino P.S., San Vito E., Carvalho I.P.C., Berchielli T.T. Effects of different forms of soybean lipids on enteric methane emission, performance and meat quality of feedlot Nellore. The Journal of Agricultural Science, 2018, 156(3): 427-436 CrossRef
  55. Roca-Fernández A.I., Dillard S.L., Soder K.J. Ruminal fermentation and enteric methane production of legumes containing condensed tannins fed in continuous culture. Journal of Dairy Science, 2020, 103(8): 7028-7038 CrossRef
  56. Ryazanov V.A., Sheyda E.V., Duskaev G.K., Rakhmatullin Sh.G., Kvan O.V. Agrarnaya nauka, 2022, 1(7-8): 86-92 CrossRef (in Russ.).
  57. Atlanderova K., Makaeva A., Rysaev A., Nurzhanov B., Duskaev G., Rayzanov V. The effect of medicinal extracts on microflora and enzymatic processes of calf rumen. Journal of Animal Science, 2020, 98(Suppl_4): 258 CrossRef
  58. Kumar R., Kumar B.A. New claims in folk veterinary medicines from Uttar Pradesh, India. J. Ethnopharmacol, 2013, 146(2): 581-593 CrossRef
  59. Cobellis G., Trabalza-Marinucci M., Yu Z. Critical evaluation of essential oils as rumen modifiers in ruminant nutrition: a review. Science of the Total Environment, 2016, 545: 556-568 CrossRef
  60. Jacondino L.R., Poli C H.E.C., Tontini J.F., Corrêa G.F., Somacal S., Mello R.O., Leal M.L.R., Raimondo R.F.S., Riet-Correa B., Muir J.P. Acacia mearnsii tannin extract and a-tocopherol supplementation in lamb diet: effects on growth performance, serum lipid peroxidation and meat quality. Animal Feed Science and Technology, 2022, 294: 115483 CrossRef
  61. Lobón S., Sanz A., Blanco M., Ripoll G., Joy M. The type of forage and condensed tannins in dams’ diet: Influence on meat shelf life of their suckling lambs. Small Ruminant Research, 2017, 154: 115-122 CrossRef
  62. Mueller-Harvey I., Bee G., Dohme-Meier F., Hoste H., Karonen M., Kölliker, R., Luscher A., Niderkorn V., Pellikaan W.F., Salminen J.P., Skot L., Smith L.M.J., Thamsborg S.M., Totterdell P., Wilkinson I., Williams A.R., Azuhnwi B.N., Baert N., Brinkhaus A.G., Copani G., Desrues O., Drake C., Engstrom M., Fryganas C., Girard M., Huyen N.T., Kempf K., Malisch C., Mora-Ortiz M., Quijada J., Ramsay A., Ropiak H.M., Waghorn G.C. Benefits of condensed tannins in forage legumes fed to ruminants: importance of structure, concentration, and diet composition. Crop Science, 2019, 59(3): 861-885 CrossRef
  63. Hoste H., Torres-Acosta J.F.J., Quijada J., Chan-Perez I., Dakheel M.M., Kommuru D.S., Mueller-Harvey I., Terrill T.H. Interactions between nutrition and infections with Haemonchus contortus and related gastrointestinal nematodes in small ruminants. Advances in Parasitology, 2016, 93: 239-351 CrossRef
  64. MacAdam J.W., Villalba J.J. Beneficial effects of temperate forage legumes that contain condensed tannins. Agriculture, 2015, 5(3): 475-491 CrossRef
  65. Junior F.P., Cassiano E.C.O., Martins M.F., Romero L.A., Zapata D.C.V., Pinedo L.A., Marino C.T., Rodrigues P.H.M. Effect of tannins-rich extract from Acacia mearnsii or monensin as feed additives on ruminal fermentation efficiency in cattle. Livestock Science, 2017, 203, 21-29 CrossRef
  66. Marshall C.J., Beck M.R., Garrett K., Castillo A.R., Barrell G.K., Al-Marashdeh O., Gregorini P. The effect of feeding a mix of condensed and hydrolyzable tannins to heifers on rumen fermentation patterns, blood urea nitrogen, and amino acid profile. Livestock Science, 2022, 263: 105034 CrossRef
  67. Makmur M., Zain M., Sholikin M.M., Suharlina, Jayanegara A. Modulatory effects of dietary tannins on polyunsaturated fatty acid biohydrogenation in the rumen: a meta-analysis. Heliyon, 2022, 8(7): e09828 CrossRef
  68. Hagerman A.E. Fifty years of polyphenol—protein complexes. In: Recent Advances in Polyphenol Research. S. Quideau, V. Cheynier, P. Sarni-Manchado, S. Quideau (eds.). John Wiley & Sons, 2012, vol. 3: 71-97 CrossRef
  69. Lima P.R., Apdini T., Freire A.S., Santana A.S., Moura L.M.L., Nascimento J.C.S., Rodrigues R.T.S., Dijkstra J., Garcez Neto A.F., Queiroz M.A.Á., Menezes D.R. 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 CrossRef
  70. Patra A.K., Saxena J. A new perspective on the use of plant secondary metabolites to inhibit methanogenesis in the rumen. Phytochemistry, 2010, 71(11-12): 1198-1222 CrossRef
  71. Terranova M., Kreuzer M., Braun U., Schwarm A. In vitro screening of temperate climate forages from a variety of woody plants for their potential to mitigate ruminal methane and ammonia formation. The Journal of Agricultural Science, 2018, 156(7): 929-941 CrossRef
  72. Rira M., Morgavi D.P., Popova M., Maxin G., Doreau, M. Microbial colonisation of tannin-rich tropical plants: interplay between degradability, methane production and tannin disappearance in the rumen. Animal, 2022, 16(8): 100589 CrossRef
  73. Naumann H.D., Tedeschi L.O., Zeller W.E., Huntley N.F. The role of condensed tannins in ruminant animal production: advances, limitations and future directions. Revista Brasileira de Zootecnia, 2017, 46(12): 929-949 CrossRef
  74. Díaz Carrasco J.M., Cabral C., Redondo L.M., Pin Viso N.D., Colombatto D., Farber M.D., Fernandez Miyakawa M.E. Impact of chestnut and quebracho tannins on rumen microbiota of bovines. BioMed Research International, 2017, 2017(3): 1-11 CrossRef
  75. Vasta V., Daghio M., Cappucci A., Buccioni A., Serra A., Viti C., Mele M. Invited review: Plant polyphenols and rumen microbiota responsible for fatty acid biohydrogenation, fiber digestion, and methane emission: experimental evidence and methodological approaches. Journal of Dairy Science, 2019, 102(5): 3781-3804 CrossRef
  76. Mannino G., Chinigò G., Serio G., Genova T., Gentile C., Munaron L., Bertea C.M. Proanthocyanidins and where to find them: a meta-analytic approach to investigate their chemistry, biosynthesis, distribution, and effect on human health. Antioxidants, 2021, 10(8): 1229 CrossRef
  77. Mannino G., Gentile C., Ertani A., Serio G., Bertea C.M. Anthocyanins: biosynthesis, distribution, ecological role, and use of biostimulants to increase their content in plant foods — a review. Agriculture, 2021, 11(3): 212 CrossRef
  78. Jayanegara A., Goel G., Makkar H.P., Becker K. 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 CrossRef
  79. Salami S.A., Valenti B., Bella M., O'Grady M.N., Luciano G., Kerry J.P., Jones E., Priolo A., Newbold C.J. Characterisation of the ruminal fermentation and microbiome in lambs supplemented with hydrolysable and condensed tannins. FEMS Microbiology Ecology, 2018, 94(5): fiy061 CrossRef
  80. Caetano M., Wilkes M.J., Pitchford W.S., Lee S.J., Hynd P.I. Effect of ensiled crimped grape marc on energy intake, performance and gas emissions of beef cattle. Animal Feed Science and Technology, 2019, 247: 166-172 CrossRef
  81. Ng F., Kittelmann S., Patchett M.L., Attwood G.T., Janssen P.H., Rakonjac J., Gagic D. An adhesin from hydrogen‐utilizing rumen methanogen M ethanobrevibacter ruminantium M 1 binds a broad range of hydrogen‐producing microorganisms. Environmental Microbiology, 2016, 18(9): 3010-3021 CrossRef
  82. Bhatta R., Saravanan M., Baruah L., Prasad C.S. Effects of graded levels of tannin‐containing tropical tree leaves on in vitro rumen fermentation, total protozoa and methane production. Journal of Applied Microbiology, 2015 118(3): 557-564 CrossRef
  83. Costa M., Alves S.P., Cabo Â., Guerreiro O., Stilwell G., Dentinho M.T., Bessa R.J. Modulation of in vitro rumen biohydrogenation by Cistus ladanifer tannins compared with other tannin sources. Journal of the Science of Food and Agriculture, 2018, 97(2): 629-635 CrossRef
  84. Cappucci A., Mantino A., Buccioni A., Casarosa L., Conte G., Serra A., Mannelli F., Luciano G., Foggi G., Mele M. Diets supplemented with condensed and hydrolysable tannins affected rumen fatty acid profile and plasmalogen lipids, ammonia and methane production in an in vitro study. Italian Journal of Animal Science, 2021, 20(1): 935-946 CrossRef
  85. Mannelli F., Daghio M., Alves S.P., Bessa R.J., Minieri S., Giovannetti L., Conte G., Mele M., Messini A., Rapaccini S., Viti C., Buccioni A. Effects of chestnut tannin extract, vescalagin and gallic acid on the dimethyl acetals profile and microbial community composition in rumen liquor: an in vitro study. Microorganisms, 2019, 7(7): 202 CrossRef
  86. Lavin S.R. Plant phenolics and their potential role in mitigating iron overload disorder in wild animals. Journal of Zoo and Wildlife Medicine, 2012, 43(3s): 74-82 CrossRef
  87. Saminathan M., Tan H.Y., Sieo C.C., Abdullah N., Wong C.M.V.L., Abdulmalek E., Ho Y.W. Polymerization degrees, molecular weights and protein-binding affinities of condensed tannin fractions from a Leucaena leucocephala hybrid. Molecules, 2014, 19(6): 7990-8010 CrossRef
  88. Min B.R., Wright C., Ho P., Eun J.-S., Gurung N., Shange R. The effect of phytochemical tannins-containing diet on rumen fermentation characteristics and microbial diversity dynamics in goats using 16S rDNA amplicon pyrosequencing. Agriculture, Food and Analytical Bacteriology, 2014, 4(195-211): 141909.
  89. Gemeda B.S., Hassen A. Effect of tannin and species variation on in vitro digestibility, gas, and methane production of tropical browse plants. Asian-Australasian Journal of Animal Sciences, 2015, 28(2): 188-199 CrossRef
  90. Li Z., Wright A.-D.G., Liu H., Fan Z., Yang F., Zhang Z., Li G. Response of the rumen microbiota of sika deer (Cervus nippon) fed different concentrations of tannin rich plants. PLoS ONE, 2015, 10(5): e0123481 CrossRef
  91. Hassanat F., Benchaar C. Assessment of the effect of condensed (acacia and quebracho) and hydrolysable (chestnut and valonea) tannins on rumen fermentation and methane production in vitro. Journal of the Science of Food and Agriculture, 2013, 93(2): 332-339 CrossRef
  92. Terranova M., Wang S., Eggerschwiler L., Braun U., Kreuzer M., Schwarm A. Dose-response effects of woody and herbaceous forage plants on in vitro ruminal methane and ammonia formation, and their short-term palatability in lactating cows. Animal, 2020, 14(3): 538-548 CrossRef
  93. Terranova M., Eggerschwiler L., Ortmann S., Clauss M., Kreuzer M., Schwarm A. Increasing the proportion of hazel leaves in the diet of dairy cows reduced methane yield and excretion of nitrogen in volatile form, but not milk yield. Animal Feed Science and Technology, 2021, 276: 114790 CrossRef
  94. Wang S., Terranova M., Kreuzer M., Marquardt S., Eggerschwiler L., Schwarm A. Supplementation of pelleted hazel (Corylus avellana) leaves decreases methane and urinary nitrogen emissions by sheep at unchanged forage intake. Scientific Reports, 2018, 8(1): 5427 CrossRef
  95. El-Zaiat H.M., Kholif A.E., Moharam M.S., Attia M.F., Abdalla A.L., Sallam S.M.A. The ability of tanniniferous legumes to reduce methane production and enhance feed utilization in Barki rams: in vitro and in vivo evaluation. Small Ruminant Research, 2020, 193: 106259 CrossRef
  96. Ku-Vera J.C., Jiménez-Ocampo R., Valencia-Salazar S.S., Montoya-Flores M.D., Molina-Botero I.C., Arango J., Gómez-Bravo C.A., Aguilar-Pérez C.F., Solorio-Sánchez F.J. Role of secondary plant metabolites on enteric methane mitigation in ruminants. Frontiers in Veterinary Science, 2020, 7: 584 CrossRef
  97. Piñeiro-Vázquez A.T., Canul-Solis J.R., Jiménez-Ferrer G.O., Alayón-Gamboa J.A., Chay-Canul A.J., Ayala-Burgos A.J., Aguilar-Pérez C.F., Ku-Vera J.C. Effect of condensed tannins from Leucaena leucocephala on rumen fermentation, methane production and population of rumen protozoa in heifers fed low-quality forage. Asian-Australasian Journal of Animal Sciences, 2018, 31(11): 1738 CrossRef
  98. Montoya-Flores M.D., Molina-Botero I.C., Arango J., Romano-Muñoz J.L., Solorio-Sánchez F.J., Aguilar-Pérez C.F., Ku-Vera J.C. Effect of dried leaves of Leucaena leucocephala on rumen fermentation, rumen microbial population, and enteric methane production in crossbred heifers. Animals, 2020, 10(2): 300 CrossRef
  99. Denninger T.M., Schwarm A., Birkinshaw A., Terranova M., Dohme-Meier F., Münger A., Eggerschwiler L., Bapst B., Wegmann S., Clauss M., Kreuzer M. Immediate effect of Acacia mearnsii tannins on methane emissions and milk fatty acid profiles of dairy cows. Animal Feed Science and Technology, 2020, 261: 114388 CrossRef
  100. Yang K., Wei C., Zhao G.Y., Xu Z.W., Lin S.X. Effects of dietary supplementing tannic acid in the ration of beef cattle on rumen fermentation, methane emission, microbial flora and nutrient digestibility. Journal of Animal Physiology and Animal Nutrition, 2017, 101(2): 302-310 CrossRef
  101. Liu H., Vaddella V., Zhou D. Effects of chestnut tannins and coconut oil on growth performance, methane emission, ruminal fermentation, and microbial populations in sheep. Journal of Dairy Science, 2011, 94(12): 6069-6077 CrossRef
  102. Bhatt R.S., Sarkar S., Sharma P., Soni L., Sahoo A. Comparing the efficacy of forage combinations with different hydrolysable and condensed tannin levels to improve production and lower methane emission in finisher lambs. Small Ruminant Research, 2023, 218: 106876 CrossRef
  103. Torres R.N.S., Ghedini C.P., Paschoaloto J.R., da Silva D.A.V., Coelho L.M., Almeida Junior G.A., Ezequiel J.M.B., Machado Neto O.R., Almeida M.T.C. Effects of tannins supplementation to sheep diets on their performance, carcass parameters and meat fatty acid profile: a meta-analysis study. Small Ruminant Research, 2022, 206: 106585 CrossRef
  104. Ibrahim S.L., Hassen A. Effect of non-encapsulated and encapsulated mimosa (Acacia mearnsii) tannins on growth performance, nutrient digestibility, methane and rumen fermentation of South African mutton Merino ram lambs. Animal Feed Science and Technology, 2022, 294: 115502 CrossRef
  105. Febres F.E.F., Terrazas L.A., Vasquez J.Ñ., Muñoz J.E.M., Howard F.S.M., Mariazza E.F. Effects of chestnut bark (Castanea spp.) tannin extracts on selectivity, dry matter intake, weight gain, and enteric methane emission from llamas (Lama glama) under grazing conditions in the high Andean grasslands. Small Ruminant Research, 2021, 205: 106559 CrossRef

 

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