Manipulation of rumen fermentation and methane production with plant secondary metabolites
Abstract
Methane produced by ruminants represents a loss of energy for ruminants and contributes to the greenhouse gas emissions which have a global warming potential. This review describes the basic conceptual aspects of ruminal methanogenesis, which is a way of keeping a low Hâ pressure in the rumen by reducing COâ, and steps where it may be possible to intervene to reduce CHâ production. Numerous studies have been completed on use of plant secondary metabolites (PSM) in substitute for chemical feed additives because some of them modify rumen fermentation and reduce CHâ production. This review aims to illustrate the multiplicity of possible effects of the major groups of PSM (i.e., saponins, tannins, essential oils) on ruminal microbiota (i.e., protozoa, fungi, bacteria), ammonia N concentration and fermentation end products (i.e., volatile fatty acids). Finally, a comprehensive review on effects of PSM on CHâ production is included, with a discussion of possible underlying mechanisms and key factors affecting the observed effects of PSM.
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Plant secondary metabolites have shown to reduce methanogenesis both in vitro and in vivo.
“They have also shown to reduce the methanogenesis both in vitro and in vivo (29, 31, 76, 148, 149).”
From Phytogenic Additives Can Modulate Rumen Microbiome to Mediate Fermentation Kinetics and Methanogenesis Through Exploiting Diet–Microbe Interaction (2020) · cites this paper as [76]
Cites
Climate change 2007: the physical science basis
Solomon, S., Qin, D., Manning, M., Marquis, M. C., Averyt, K. B., Tignor, M., Miller, H. L., & Chen, Z. (2007) · Cited by 23,398 · see citing works
Climate change 2001 : the scientific basis
Houghton, J., Ding, Y., Griggs, D., Noguer, M., van der Linden, P. V. D., Dai, X., Maskell, K., & Johnson, C. (2001) · Foreign Affairs · doi:10.2307/20033020 · Cited by 14,162 · see citing works
Essential oils: Their antibacterial properties and potential applications in foods—A review
Burt, S. (2004) · International Journal of Food Microbiology · doi:10.1016/j.ijfoodmicro.2004.03.022 · Cited by 10,488 · see citing works
Plant Products as Antimicrobial Agents
Cowan, M. M. (1999) · Clinical Microbiology Reviews · doi:10.1128/cmr.12.4.564 · Cited by 9,043 · see citing works
Biological effects of essential oils—A review
Bakkali, F., Averbeck, S., Averbeck, D., & Idaomar, M. (2008) · Food and Chemical Toxicology · doi:10.1016/j.fct.2007.09.106 · Cited by 7,929 · see citing works
Livestock's long shadow: environmental issues and options.
Steinfeld, H., Gerber, P., Wassenaar, T., Castel, V., Rosales, M., & de Haan, C. (2006) · Agritrop (Cirad) · Cited by 4,383 · see citing works
Antimicrobial agents from plants: Antibacterial activity of plant volatile oils
Dorman, H. J. D., & Deans, S. G. (2000) · Journal of Applied Microbiology · doi:10.1046/j.1365-2672.2000.00969.x · Cited by 4,334 · see citing works
Hungate, R. E. (2013) · Elsevier eBooks · doi:10.1016/c2013-0-12555-x · Cited by 3,060 · see citing works
Inventory of U.S. Greenhouse Gas Emissions and Sinks
Hockstad, L., & Hanel, L. (2018) · University of North Texas Digital Library (University of North Texas) · doi:10.15485/1464240 · Cited by 2,861 · see citing works
Rebitzer, G., Ekvall, T., Frischknecht, R., Hunkeler, D., Norris, G., Rydberg, T., Schmidt, W.-P., Suh, S., Weidema, B. P., & Pennington, D. W. (2004) · Environment International · doi:10.1016/j.envint.2003.11.005 · Cited by 2,753 · see citing works
Johnson, K. A., & Johnson, D. E. (1995) · Journal of Animal Science · doi:10.2527/1995.7382483x · Cited by 2,714 · see citing works
Framework convention on climate change
Venanzi, M. (1992) · Cited by 2,585 · see citing works
Hobson, P. N., & Stewart, C. S. (1997) · Springer eBooks · doi:10.1007/978-94-009-1453-7 · Cited by 2,146 · see citing works
The biological action of saponins in animal systems: a review
Francis, G., Kerem, Z., Makkar, H. P. S., & Becker, K. (2002) · British Journal Of Nutrition · doi:10.1079/bjn2002725 · Cited by 1,722 · see citing works
Characterization of the action of selected essential oil components on Gram-negative bacteria
Helander, I. M., Alakomi, H.-L., Latva-Kala, K., Mattila-Sandholm, T., Pol, I., Smid, E. J., Gorris, L. G. M., & von Wright, A. (1998) · Journal of Agricultural and Food Chemistry · doi:10.1021/jf980154m · Cited by 1,664 · see citing works
Recent Advances in Animal Nutrition – 1979
(1980) · Elsevier eBooks · doi:10.1016/c2013-0-04245-4 · Cited by 1,618 · see citing works
Ultee, A., Bennik, M. H. J., & Moezelaar, R. (2002) · Applied and Environmental Microbiology · doi:10.1128/aem.68.4.1561-1568.2002 · Cited by 1,602 · see citing works
Prevention of Drug Access to Bacterial Targets: Permeability Barriers and Active Efflux
Nikaido, H. (1994) · Science · doi:10.1126/science.8153625 · Cited by 1,542 · see citing works
Consequences of climate change for European agricultural productivity, land use and policy
Olesen, J. E., & Bindi, M. (2002) · European Journal of Agronomy · doi:10.1016/s1161-0301(02)00004-7 · Cited by 1,469 · see citing works
Methane production by ruminants: its contribution to global warming
Moss, A. R., Jouany, J.-P., & Newbold, J. (2000) · Annales de Zootechnie · doi:10.1051/animres:2000119 · Cited by 1,414 · see citing works
Digestion and metabolism in the ruminant.
McDonald, I. W., & Warner, A. C. I. (1975) · Cited by 1,164 · see citing works
Nutritional management for enteric methane abatement: a review
Beauchemin, K. A., Kreuzer, M., O’Mara, F. P., & McAllister, T. A. (2008) · Australian Journal of Experimental Agriculture · doi:10.1071/ea07199 · Cited by 1,162 · see citing works
Invited review: essential oils as modifiers of rumen microbial fermentation
Calsamiglia, S., Busquet, M., Cardozo, P. W., Castillejos, L., & Ferret, A. (2007) · Journal of Dairy Science · doi:10.3168/jds.2006-644 · Cited by 1,014 · see citing works
Pharmacognosy, Phytochemistry, Medicinal Plants
Schmid, R., Bruneton, J., & Hatton, C. K. (1995) · Taxon · doi:10.2307/1223435 · Cited by 911 · see citing works
Methane mitigation in ruminants: from microbe to the farm scale
Martin, C., Morgavi, D. P., & Doreau, M. (2009) · animal · doi:10.1017/s1751731109990620 · Cited by 887 · see citing works
Janssen, P. H. (2010) · Animal Feed Science and Technology · doi:10.1016/j.anifeedsci.2010.07.002 · Cited by 848 · see citing works
Exploitation of dietary tannins to improve rumen metabolism and ruminant nutrition
Patra, A. K., & Saxena, J. (2010) · Journal of the Science of Food and Agriculture · doi:10.1002/jsfa.4152 · Cited by 837 · see citing works
From waste products to ecochemicals: Fifty years research of plant secondary metabolism
Hartmann, T. (2007) · Phytochemistry · doi:10.1016/j.phytochem.2007.09.017 · Cited by 798 · see citing works
Stewart, C. S., Flint, H. J., & Bryant, M. P. (1997) · The Rumen Microbial Ecosystem · doi:10.1007/978-94-009-1453-7_2 · Cited by 772 · see citing works
Waghorn, G. C. (2007) · Animal Feed Science and Technology · doi:10.1016/j.anifeedsci.2007.09.013 · Cited by 738 · see citing works
Biotechnology in the feed industry
Lyons, T. (1987) · Cited by 703 · see citing works
Natural Food Antimicrobial Systems
(2000) · CRC Press eBooks · doi:10.1201/9781420039368 · Cited by 692 · see citing works
A review of plant-derived essential oils in ruminant nutrition and production
Benchaar, C., Calsamiglia, S., Chaves, A. V., Fraser, G. R., Colombatto, D., McAllister, T. A., & Beauchemin, K. A. (2007) · Animal Feed Science and Technology · doi:10.1016/j.anifeedsci.2007.04.014 · Cited by 636 · see citing works
A new perspective on the use of plant secondary metabolites to inhibit methanogenesis in the rumen
Patra, A. K., & Saxena, J. (2010) · Phytochemistry · doi:10.1016/j.phytochem.2010.05.010 · Cited by 595 · see citing works
Options for the abatement of methane and nitrous oxide from ruminant production: A review
Eckard, R., Grainger, C. I., & de Klein, C. A. M. (2010) · Livestock Science · doi:10.1016/j.livsci.2010.02.010 · Cited by 595 · see citing works
The environmental impact of dairy production: 1944 compared with 20071
Capper, J. L., Cady, R., & Bauman, D. E. (2009) · Journal of Animal Science · doi:10.2527/jas.2009-1781 · Cited by 595 · see citing works
Methanogens: Methane Producers of the Rumen and Mitigation Strategies
Hook, S. E., Wright, A. G., & McBride, B. W. (2010) · Archaea · doi:10.1155/2010/945785 · Cited by 565 · see citing works
Tavendale, M. H., Meagher, L. P., Pacheco, D., Walker, N. D., Attwood, G. T., & Sivakumaran, S. (2005) · Animal Feed Science and Technology · doi:10.1016/j.anifeedsci.2005.04.037 · Cited by 541 · see citing works
Review. Tannins and ruminant nutrition
Frutos, P., Hervás, G., Giráldez, F. J., & Mantecón, Á. R. (2004) · Spanish Journal of Agricultural Research · doi:10.5424/sjar/2004022-73 · Cited by 518 · see citing works
Self-citationRedirecting rumen fermentation to reduce methanogenesis
McAllister, T. A., & Newbold, C. J. (2008) · Australian Journal of Experimental Agriculture · doi:10.1071/ea07218 · Cited by 501 · see citing works
Antimicrobial properties of plant secondary metabolites
Wallace, R. J. (2004) · Proceedings of The Nutrition Society · doi:10.1079/pns2004393 · Cited by 492 · see citing works
Makkar, H. P. S., Francis, G., & Becker, K. (2007) · animal · doi:10.1017/s1751731107000298 · Cited by 491 · see citing works
A Theoretical Rumen Fermentation Balance
Wolin, M. J. (1960) · Journal of Dairy Science · doi:10.3168/jds.s0022-0302(60)90348-9 · Cited by 484 · see citing works
Plant Extracts Affect In Vitro Rumen Microbial Fermentation
Busquet, M., Calsamiglia, S., Ferret, A., & Kamel, C. (2006) · Journal of Dairy Science · doi:10.3168/jds.s0022-0302(06)72137-3 · Cited by 482 · see citing works
Microbial Methane Production—Theoretical Aspects2
Bryant, M. P. (1979) · Journal of Animal Science · doi:10.2527/jas1979.481193x · Cited by 469 · see citing works
Terpenoids as Plant Antioxidants
Graßmann, J. (2005) · Vitamins and hormones · doi:10.1016/s0083-6729(05)72015-x · Cited by 466 · see citing works
Ecology and evolution in anoxic worlds
Fenchel, T., & Finlay, B. J. (1996) · Choice Reviews Online · doi:10.5860/choice.33-2713 · Cited by 459 · see citing works
Energy Metabolism of Farm Animals
van Es, A. J. H., & Boekholt, H. A. (1987) · Springer eBooks · doi:10.1007/978-94-009-3363-7_1 · Cited by 448 · see citing works
Use of condensed tannin extract from quebracho trees to reduce methane emissions from cattle1
Beauchemin, K. A., McGinn, S. M., Martínez, T. F., & McAllister, T. A. (2007) · Journal of Animal Science · doi:10.2527/jas.2006-686 · Cited by 418 · see citing works
Effects of essential oils on ruminal microorganisms and their protein metabolism
McIntosh, F. M., Williams, P., Losa, R., Wallace, R. J., Beever, D. A., & Newbold, C. J. (2003) · Applied and Environmental Microbiology · doi:10.1128/aem.69.8.5011-5014.2003 · Cited by 412 · see citing works
Biochemistry of plant secondary metabolites and their effects in animals
Acamovic, T., & Brooker, J. D. (2005) · Proceedings of The Nutrition Society · doi:10.1079/pns2005449 · Cited by 395 · see citing works
Methane emissions from beef cattle: Effects of fumaric acid, essential oil, and canola oil1
Beauchemin, K. A., & McGinn, S. M. (2006) · Journal of Animal Science · doi:10.2527/2006.8461489x · Cited by 379 · see citing works
Greenhouse gas abatement strategies for animal husbandry
Monteny, G. J., Bannink, A., & Chadwick, D. R. (2005) · Agriculture Ecosystems & Environment · doi:10.1016/j.agee.2005.08.015 · Cited by 373 · see citing works
Structure, biosynthesis, and physicochemical properties of archaebacterial lipids
ROSA, M. D., Gambacorta, A., & Gliozzi, A. (1986) · Microbiological Reviews · doi:10.1128/mr.50.1.70-80.1986 · Cited by 372 · see citing works
Plants and plant extracts for improving animal productivity
Greathead, H. M. R. (2003) · Proceedings of The Nutrition Society · doi:10.1079/pns2002197 · Cited by 366 · see citing works
Bhatta, R., Uyeno, Y., Tajima, K., Takenaka, A., Yabumoto, Y., Nonaka, I., Enishi, O., & Kurihara, M. (2009) · Journal of Dairy Science · doi:10.3168/jds.2008-1441 · Cited by 359 · see citing works
Essential oils and opportunities to mitigate enteric methane emissions from ruminants
Benchaar, C., & Greathead, H. M. R. (2011) · Animal Feed Science and Technology · doi:10.1016/j.anifeedsci.2011.04.024 · Cited by 357 · see citing works
Ionophore resistance of ruminal bacteria and its potential impact on human health
Russell, J. B., & Houlihan, A. J. (2003) · FEMS Microbiology Reviews · doi:10.1016/s0168-6445(03)00019-6 · Cited by 357 · see citing works
Benchaar, C., Petit, H. V., Berthiaume, R., Ouellet, D. R., Chiquette, J., & Chouinard, P. Y. (2007) · Journal of Dairy Science · doi:10.3168/jds.s0022-0302(07)71572-2 · Cited by 354 · see citing works
Castillejos, L., Calsamiglia, S., & Ferret, A. (2006) · Journal of Dairy Science · doi:10.3168/jds.s0022-0302(06)72341-4 · Cited by 344 · see citing works
Dietary phytochemicals as rumen modifiers: a review of the effects on microbial populations
Patra, A. K., & Saxena, J. (2009) · Antonie van Leeuwenhoek · doi:10.1007/s10482-009-9364-1 · Cited by 338 · see citing works
Methane mitigation from ruminants using tannins and saponins
Goel, G., & Makkar, H. P. S. (2012) · Tropical Animal Health and Production · doi:10.1007/s11250-011-9966-2 · Cited by 336 · see citing works
Use of ‘natural’ products as alternatives to antibiotic feed additives in ruminant production
Jouany, J. P., & Morgavi, D. P. (2007) · animal · doi:10.1017/s1751731107000742 · Cited by 328 · see citing works
Natural products as manipulators of rumen fermentation
Wallace, R. J., McEwan, N. R., McIntosh, F. M., Teferedegne, B., & Newbold, C. J. (2002) · Asian-Australasian Journal of Animal Sciences · doi:10.5713/ajas.2002.1458 · Cited by 324 · see citing works
Patra, A. K., & Saxena, J. (2009) · Nutrition Research Reviews · doi:10.1017/s0954422409990163 · Cited by 323 · see citing works
Mitigating climate change: the role of domestic livestock
Gill, M., Smith, P., & Wilkinson, J. M. (2009) · animal · doi:10.1017/s1751731109004662 · Cited by 319 · see citing works
Plant secondary metabolites: occurrence, structure and role in the human diet
Smith, E. C. J. (2007) · Phytotherapy Research · doi:10.1002/ptr.2237 · Cited by 317 · see citing works
Newton, S. M., Lau, C. B., Gurcha, S. S., Besra, G. S., & Wright, C. W. (2002) · Journal of Ethnopharmacology · doi:10.1016/s0378-8741(01)00350-6 · Cited by 316 · see citing works
Bacterial Mechanisms to Overcome Inhibitory Effects of Dietary Tannins
Smith, A. H., Zoetendal, E. G., & Mackie, R. I. (2005) · Microbial Ecology · doi:10.1007/s00248-004-0180-x · Cited by 314 · see citing works
Plant extracts to manipulate rumen fermentation
Hart, K. J., Yáñez-Ruiz, D. R., Duval, S. M., McEwan, N. R., & Newbold, C. J. (2008) · Animal Feed Science and Technology · doi:10.1016/j.anifeedsci.2007.09.007 · Cited by 314 · see citing works
Natural Food Antimicrobial Systems
(2000) · CRC Press eBooks · doi:10.1201/9780367801779 · Cited by 298 · see citing works
Cardozo, P. W., Calsamiglia, S., Ferret, A., & Kamel, C. (2005) · Journal of Animal Science · doi:10.2527/2005.83112572x · Cited by 296 · see citing works
Third assessment report of the Intergovernmental Panel on Climate Change
Australia, Azerbaijan, Bolívia, et al. (2002) · Cited by 293 · see citing works
In vitro effects of and interactions between tannins and saponins and fate of tannins in the rumen
Makkar, H. P. S., Blümmel, M., & Becker, K. (1995) · Journal of the Science of Food and Agriculture · doi:10.1002/jsfa.2740690413 · Cited by 290 · see citing works
Evaluation of dietary strategies to reduce methane production in ruminants: A modelling approach
Benchaar, C., Pomar, C., & Chiquette, J. (2001) · Canadian Journal of Animal Science · doi:10.4141/a00-119 · Cited by 288 · see citing works
Plant Secondary Metabolites: Occurrence, Structure And Role In The Human Diet
Crozier, A., Clifford, M. B., & Ashihara, H. (2014) · Wiley eBooks · doi:10.1002/9780470988558 · Cited by 287 · see citing works
Pharmacognosy: Phytochemistry, Medicinal Plants
Ernst, E. K. (2000) · Focus on Alternative and Complementary Therapies · doi:10.1111/j.2042-7166.2000.tb02451.x · Cited by 287 · see citing works
Phenols, Polyphenols and Tannins: An Overview
Crozier, A., Jaganath, I. B., & Clifford, M. N. (2006) · doi:10.1002/9780470988558.ch1 · Cited by 286 · see citing works
Recent advances in animal nutrition
van Es, A. J. H. (1987) · Livestock Production Science · doi:10.1016/0301-6226(87)90074-1 · Cited by 271 · see citing works
Cardozo, P. W., Calsamiglia, S., Ferret, A., & Kamel, C. (2004) · Journal of Animal Science · doi:10.2527/2004.82113230x · Cited by 269 · see citing works
Patra, A. K. (2012) · Environmental Monitoring and Assessment · doi:10.1007/s10661-011-2090-y · Cited by 263 · see citing works
Effect of Yucca schidigera on ruminal fermentation and nutrient digestion in heifers.
Hristov, A. N., McAllister, T. A., Herk, F. H. V., Cheng, K. J., Newbold, C. J., & Cheeke, P. R. (1999) · Journal of Animal Science · doi:10.2527/1999.7792554x · Cited by 262 · see citing works
Effects of a specific blend of essential oil compounds on rumen fermentation
Newbold, C. J., McIntosh, F. M., Williams, P., Losa, R., & Wallace, R. J. (2004) · Animal Feed Science and Technology · doi:10.1016/j.anifeedsci.2003.12.006 · Cited by 255 · see citing works
Mills, J. A. N., Dijkstra, J., Bannink, A., Cammell, S. B., Kebreab, E., & France, J. (2001) · Journal of Animal Science · doi:10.2527/2001.7961584x · Cited by 253 · see citing works
Influence of Yucca shidigera extract on ruminal ammonia concentrations and ruminal microorganisms
Wallace, R. J., Arthaud, L., & Newbold, C. J. (1994) · Applied and Environmental Microbiology · doi:10.1128/aem.60.6.1762-1767.1994 · Cited by 252 · see citing works
Tan, H. Y., Sieo, C. C., Abdullah, N., Liang, J. B., Huang, X. D., & Ho, Y. W. (2011) · Animal Feed Science and Technology · doi:10.1016/j.anifeedsci.2011.07.004 · Cited by 243 · see citing works
Busquet, M., Calsamiglia, S., Ferret, A., Cardozo, P. W., & Kamel, C. (2005) · Journal of Dairy Science · doi:10.3168/jds.s0022-0302(05)72928-3 · Cited by 241 · see citing works
Influence of foliage from African multipurpose trees on activity of rumen protozoa and bacteria
Newbold, C. J., El Hassan, S. M., Wang*, J., Ortega, M. E., & Wallace, R. J. (1997) · British Journal Of Nutrition · doi:10.1079/bjn19970143 · Cited by 238 · see citing works
Effect of Rumen Protozoa on Nitrogen Utilization by Ruminants
Jouany, J. P. (1996) · Journal of Nutrition · doi:10.1093/jn/126.suppl_4.1335s · Cited by 229 · see citing works
Cardozo, P. W., Calsamiglia, S., Ferret, A., & Kamel, C. (2006) · Journal of Animal Science · doi:10.2527/jas.2005-593 · Cited by 229 · see citing works
Hess, H. D., Kreuzer, M., Díaz, T. E., Lascano, C. E., Carulla, J. E., Soliva, C. R., & Machmüller, A. (2003) · Animal Feed Science and Technology · doi:10.1016/s0377-8401(03)00212-8 · Cited by 226 · see citing works
Structure, biosynthesis, and physicochemical properties of archaebacterial lipids.
Rosa, M. D., Gambacorta, A., & Gliozzi, A. (1986) · Microbiological Reviews · doi:10.1128/mmbr.50.1.70-80.1986 · Cited by 219 · see citing works
Machebœuf, D., Morgavi, D. P., Papon, Y., Mousset, J. L., & Schaan, M. A. (2007) · Animal Feed Science and Technology · doi:10.1016/j.anifeedsci.2007.05.044 · Cited by 212 · see citing works
Ramírez-Restrepo, C. A., & Barry, T. N. (2005) · Animal Feed Science and Technology · doi:10.1016/j.anifeedsci.2005.01.015 · Cited by 198 · see citing works
Energy-yielding and energy-consuming reactions
Russell, J. B., & Wallace, R. J. (1997) · Springer eBooks · doi:10.1007/978-94-009-1453-7_6 · Cited by 190 · see citing works
Goel, G., Makkar, H. P. S., & Becker, K. (2008) · Animal Feed Science and Technology · doi:10.1016/j.anifeedsci.2007.09.010 · Cited by 189 · see citing works
Methane Prediction in Dry and Lactating Holstein Cows
Holter, J. B., & Young, A. J. (1992) · Journal of Dairy Science · doi:10.3168/jds.s0022-0302(92)77976-4 · Cited by 185 · see citing works
Czerkawski, J. W., Blaxter, K. L., & Wainman, F. W. (1966) · British Journal Of Nutrition · doi:10.1079/bjn19660035 · Cited by 182 · see citing works
Wang, Y., McAllister, T. A., Newbold, C. J., Rode, L. M., Cheeke, P. R., & Cheng, K.-J. (1998) · Animal Feed Science and Technology · doi:10.1016/s0377-8401(98)00137-0 · Cited by 177 · see citing works
Reducing methane emissions in sheep by immunization against rumen methanogens
WRIGHT, A. (2004) · Vaccine · doi:10.1016/j.vaccine.2004.03.053 · Cited by 176 · see citing works
Effects of Essential Oils on Rumen Fermentation, Microbial Ecology and Ruminant Production
Patra, A. K. (2011) · Asian Journal of Animal and Veterinary Advances · doi:10.3923/ajava.2011.416.428 · Cited by 172 · see citing works
Alfalfa Saponins Affect Site and Extent of Nutrient Digestion in Ruminants
Lu, C. D., & Jorgensen, N. A. (1987) · Journal of Nutrition · doi:10.1093/jn/117.5.919 · Cited by 164 · see citing works
Bodas, R., López, S., Fernández, M., García-González, R., Rodríguez, A. B., Wallace, R. J., & González, J. S. (2007) · Animal Feed Science and Technology · doi:10.1016/j.anifeedsci.2007.04.015 · Cited by 164 · see citing works
Self-citationRumen protozoa and methanogenesis: not a simple cause–effect relationship
Morgavi, D. P., Martin, C., Jouany, J. P., & Ranilla, M. J. (2011) · British Journal Of Nutrition · doi:10.1017/s0007114511002935 · Cited by 163 · see citing works
Hess, H. D., Monsalve, L. M., Lascano, C. E., Carulla, J. E., Díaz, T. E., & Kreuzer, M. (2003) · Australian Journal of Agricultural Research · doi:10.1071/ar02241 · Cited by 162 · see citing works
Energy metabolism of farm animals
Corbett, J. L. (1990) · Animal Feed Science and Technology · doi:10.1016/0377-8401(90)90167-7 · Cited by 162 · see citing works
Efficacy of plant extracts rich in secondary constituents to modify rumen fermentation
Śliwiński, B., Soliva, C. R., Machmüller, A., & Kreuzer, M. (2002) · Animal Feed Science and Technology · doi:10.1016/s0377-8401(02)00139-6 · Cited by 161 · see citing works
Effects of essential oils and their components on in vitro rumen microbial fermentation
Benchaar, C., Chaves, A. V., Fraser, G. R., Beauchemin, K. A., & McAllister, T. A. (2007) · Canadian Journal of Animal Science · doi:10.4141/cjas07012 · Cited by 161 · see citing works
Jayanegara, A., Wina, E., Soliva, C. R., Marquardt, S., Kreuzer, M., & Leiber, F. (2010) · Animal Feed Science and Technology · doi:10.1016/j.anifeedsci.2010.11.009 · Cited by 159 · see citing works
Ruminal acetogens and their potential to lower ruminant methane emissions.
Joblin, K. N. (1999) · Australian Journal of Agricultural Research · doi:10.1071/ar99004 · Cited by 159 · see citing works
Effects of alfalfa root saponins on digestive function in sheep.
Klita, P. T., Mathison, G. W., Fenton, T. W., et al. (1996) · Journal of Animal Science · doi:10.2527/1996.7451144x · Cited by 158 · see citing works
Goel, G., Makkar, H. P. S., & Becker, K. (2008) · Journal of Applied Microbiology · doi:10.1111/j.1365-2672.2008.03818.x · Cited by 157 · see citing works
Castillejos, L., Calsamiglia, S., Ferret, A., & Losa, R. (2005) · Animal Feed Science and Technology · doi:10.1016/j.anifeedsci.2004.12.008 · Cited by 156 · see citing works
The ABC Clinical Guide to Herbs
Blumenthal, M. (2003) · Cited by 150 · see citing works
Lila, Z. A., Mohammed, N., KANDA, S., Kamada, T., & Itabashi, H. (2003) · Journal of Dairy Science · doi:10.3168/jds.s0022-0302(03)73935-6 · Cited by 146 · see citing works
Effect of the tropical forage calliandra on microbial protein synthesis and ecology in the rumen
McSweeney, C. S., Palmer, B., Bunch, R. J., & Krause, D. O. (2001) · Journal of Applied Microbiology · doi:10.1046/j.1365-2672.2001.01220.x · Cited by 146 · see citing works
New perspectives on the use of tropical plants to improve ruminant nutrition
Teferedegne, B. (2000) · Proceedings of The Nutrition Society · doi:10.1017/s0029665100000239 · Cited by 133 · see citing works
McAllister, T. A., Martínez, T. F., Bae, H. D., Muir, A. D., Yanke, L. J., & Jones, G. A. (2005) · Journal of Chemical Ecology · doi:10.1007/s10886-005-6077-4 · Cited by 129 · see citing works
Chaves, A. V., He, M. L., Yang, W., Hristov, A. N., McAllister, T. A., & Benchaar, C. (2008) · Canadian Journal of Animal Science · doi:10.4141/cjas07061 · Cited by 129 · see citing works
Castillejos, L., Calsamiglia, S., Ferret, A., & Losa, R. (2006) · Animal Feed Science and Technology · doi:10.1016/j.anifeedsci.2006.03.023 · Cited by 127 · see citing works
Liu, H., Vaddella, V., & Zhou, D. (2011) · Journal of Dairy Science · doi:10.3168/jds.2011-4508 · Cited by 126 · see citing works
Screening the activity of plants and spices for decreasing ruminal methane production in vitro
García-González, R., López, S., Fernández, M., Bodas, R., & González, J. S. (2007) · Animal Feed Science and Technology · doi:10.1016/j.anifeedsci.2007.09.008 · Cited by 123 · see citing works
Self-citationBroudiscou, L.-P., Papon, Y., & Broudiscou, A. F. (2000) · Animal Feed Science and Technology · doi:10.1016/s0377-8401(00)00193-0 · Cited by 122 · see citing works
Mathieu, F., Jouany, J., Sénaud, J., Bohatier, J., Bertin, G., & Mercier, M. (1996) · Reproduction Nutrition Development · doi:10.1051/rnd:19960305 · Cited by 119 · see citing works
Methane emission by goats consuming different sources of condensed tannins
Animut, G. M., Puchała, R., Goetsch, A. L., Patra, A. K., Sahlu, T., Varel, V. H., & Wells, J. E. (2008) · Animal Feed Science and Technology · doi:10.1016/j.anifeedsci.2007.10.015 · Cited by 119 · see citing works
Evidence of Increased Diversity of Methanogenic Archaea with Plant Extract Supplementation
Ohene-Adjei, S., Chaves, A. V., McAllister, T. A., Benchaar, C., Teather, R. M., & Forster, R. J. (2007) · Microbial Ecology · doi:10.1007/s00248-007-9340-0 · Cited by 119 · see citing works
Methane Production of Different Forages in In vitro Ruminal Fermentation
Meale, S. J., Chaves, A. V., Baah, J., & McAllister, T. A. (2011) · Asian-Australasian Journal of Animal Sciences · doi:10.5713/ajas.2011.11249 · Cited by 118 · see citing works
Wina, E., Muetzel, S., Hoffmann, E. M., Makkar, H. P. S., & Becker, K. (2005) · Animal Feed Science and Technology · doi:10.1016/j.anifeedsci.2005.02.016 · Cited by 117 · see citing works
Effect of adding acetogenic bacteria on methane production by mixed rumen microorganisms
López, S., McIntosh, F. M., Wallace, R. J., & Newbold, C. J. (1999) · Animal Feed Science and Technology · doi:10.1016/s0377-8401(98)00273-9 · Cited by 112 · see citing works
Self-citationPellikaan, W. F., Stringano, E., Leenaars, J., Bongers, D. J. G. M., Schuppen, S. V. L.-V., Plant, J., & Mueller-Harvey, I. (2011) · Animal Feed Science and Technology · doi:10.1016/j.anifeedsci.2011.04.072 · Cited by 108 · see citing works
Miller, T. L., & Wolin, M. J. (2001) · Journal of Dairy Science · doi:10.3168/jds.s0022-0302(01)70177-4 · Cited by 107 · see citing works
Vercoe, P. E., Makkar, H. P. S., & Schlink, A. C. (2009) · Springer eBooks · doi:10.1007/978-90-481-3297-3 · Cited by 104 · see citing works
Hussain, I., & Cheeke, P. R. (1995) · Animal Feed Science and Technology · doi:10.1016/0377-8401(94)00694-5 · Cited by 102 · see citing works
Effect of peppermint feeding on the digestibility, ruminal fermentation and protozoa
Sada, A. N. D. O., Nishida, T., Ishida, M., Hosoda, K., & Bayaru, E. (2003) · Livestock Production Science · doi:10.1016/s0301-6226(03)00012-5 · Cited by 99 · see citing works
Okuda, T., MORI, K., & Hatano, T. (1985) · Chemical and Pharmaceutical Bulletin · doi:10.1248/cpb.33.1424 · Cited by 99 · see citing works
Does the complexity of the rumen microbial ecology preclude methane mitigation?
Wright, A. G., & Klieve, A. V. (2011) · Animal Feed Science and Technology · doi:10.1016/j.anifeedsci.2011.04.015 · Cited by 95 · see citing works
Soliva, C. R., Zeleke, A. B., Clément, C., Hess, H. D., Fievez, V., & Kreuzer, M. (2008) · Animal Feed Science and Technology · doi:10.1016/j.anifeedsci.2007.09.009 · Cited by 93 · see citing works
Evaluation of several potential bioactive agents for reducing protozoal activity in vitro
Hristov, A. N., Ivan, M., Neill, L., & McAllister, T. A. (2003) · Animal Feed Science and Technology · doi:10.1016/s0377-8401(03)00060-9 · Cited by 93 · see citing works
Kamra, D. N., Patra, A. K., Chatterjee, P. N., Kumar, R., Agarwal, N., & Chaudhary, L. C. (2008) · Australian Journal of Experimental Agriculture · doi:10.1071/ea07268 · Cited by 92 · see citing works
Potential of phytofactors to mitigate rumen ammonia and methane production
Szumacher-Strabel, M., & Cieślak, A. (2010) · Journal of Animal and Feed Sciences · doi:10.22358/jafs/66296/2010 · Cited by 90 · see citing works
Soliva, C. R., Amelchanka, S. L., Duval, S. M., & Kreuzer, M. (2011) · British Journal Of Nutrition · doi:10.1017/s0007114510005684 · Cited by 90 · see citing works
Strategic use of tannins as means to limit methane emission from ruminant livestock
Hess, H. D., Tiemann, T. T., Noto, F., Carulla, J. E., & Kreuzer, M. (2006) · International Congress Series · doi:10.1016/j.ics.2006.01.010 · Cited by 88 · see citing works
Abdalla, A. L., Louvandini, H., Sallam, S. M. A., Bueno, I. C. D. S., Tsai, S. M., & Figueira, A. (2011) · Tropical Animal Health and Production · doi:10.1007/s11250-011-9992-0 · Cited by 87 · see citing works
Effect of Steroidal Sapogenins on Ruminal Fermentation and on Production of Lactating Dairy Cows
Valdez, F. R., Bush, L. J., Goetsch, A. L., & Owens, F. N. (1986) · Journal of Dairy Science · doi:10.3168/jds.s0022-0302(86)80573-2 · Cited by 84 · see citing works
Killeen, G. F., Madigan, C. A., Connolly, C., et al. (1998) · Journal of Agricultural and Food Chemistry · doi:10.1021/jf970928j · Cited by 83 · see citing works
A meta-analysis of fumarate effects on methane production in ruminal batch cultures
Ungerfeld, E. M., Kohn, R. A., Wallace, R. J., & Newbold, C. J. (2007) · Journal of Animal Science · doi:10.2527/jas.2006-674 · Cited by 80 · see citing works
Fandiño, J. I., Calsamiglia, S., Ferret, A., & Blanch, M. (2007) · Animal Feed Science and Technology · doi:10.1016/j.anifeedsci.2007.04.018 · Cited by 78 · see citing works
Ferris, C. P., Gordon, F. J., Patterson, D. C., Porter, M. G., & Yan, T. (1999) · The Journal of Agricultural Science · doi:10.1017/s0021859699006553 · Cited by 77 · see citing works
Durmic, Z., Hutton, P., Revell, D., Emms, J., Hughes, S., & Vercoe, P. E. (2010) · Animal Feed Science and Technology · doi:10.1016/j.anifeedsci.2010.07.006 · Cited by 74 · see citing works
Ferme, D., Banjac, M., Calsamiglia, S., Busquet, M., Kamel, C., & Avguštin, G. (2004) · Folia Microbiologica · doi:10.1007/bf02931391 · Cited by 73 · see citing works
Alexander, G., Singh, B., SAHOO, A., et al. (2007) · Animal Feed Science and Technology · doi:10.1016/j.anifeedsci.2007.05.036 · Cited by 72 · see citing works
Archaeal symbionts and parasites
Moissl‐Eichinger, C., & Huber, H. (2011) · Current Opinion in Microbiology · doi:10.1016/j.mib.2011.04.016 · Cited by 72 · see citing works
In vitro inhibition of microbial methane production by 9,10-anthraquinone.
García‐López, P. M., Kung, L., & Odom, J. M. (1996) · Journal of Animal Science · doi:10.2527/1996.7492276x · Cited by 71 · see citing works
Screening Plants and Plant Products for Methane Inhibitors
López, S., Makkar, H. P. S., & Soliva, C. R. (2009) · Springer eBooks · doi:10.1007/978-90-481-3297-3_10 · Cited by 69 · see citing works
Self-citationMonforte-Briceño, G. E., Sandoval-Castro, C. A., Ramírez-Avilés, L., & Capetillo-Leal, C. M. (2005) · Animal Feed Science and Technology · doi:10.1016/j.anifeedsci.2005.04.016 · Cited by 69 · see citing works
Mechanisms for competitively reducing ruminal methanogenesis
Hegarty, R. S. (1999) · Australian Journal of Agricultural Research · doi:10.1071/ar99007 · Cited by 66 · see citing works
Effects of a blend of essential oils on some end products of in vitro rumen fermentation
Spanghero, M., Zanfi, C., Fabbro, E., Scicutella, N., & Camellini, C. (2007) · Animal Feed Science and Technology · doi:10.1016/j.anifeedsci.2007.05.048 · Cited by 65 · see citing works
Hervás, G., Frutos, P., SERRANO, E., et al. (2000) · The Journal of Agricultural Science · doi:10.1017/s0021859699008151 · Cited by 63 · see citing works
Alternatives to Antimicrobial Growth Promoters in Cattle
Calsamiglia, S., Castillejos, L., & Busquet, M. (2006) · Recent Advances in Animal Nutrition · doi:10.5661/recadv-05-129 · Cited by 58 · see citing works
Castro-Montoya, J. M., Makkar, H. P. S., & Becker, K. (2011) · Canadian Journal of Animal Science · doi:10.4141/cjas2010-028 · Cited by 55 · see citing works
SIROHI, S. K., Pandey, N., Singh, B., & Puniya, A. K. (2010) · Indian Journal of Microbiology · doi:10.1007/s12088-010-0061-6 · Cited by 52 · see citing works
Effects of Leucaena condensed tannins of differing molecular weights on in vitro CH4 production
Huang, X. D., Liang, J. B., Tan, H. Y., Yahya, R. B., & Ho, Y. W. (2011) · Animal Feed Science and Technology · doi:10.1016/j.anifeedsci.2011.04.026 · Cited by 48 · see citing works
Jahani-Azizabadi, H. (2011) · African Journal of Microbiology Research · doi:10.5897/ajmr11.575 · Cited by 45 · see citing works
García-González, R., López, S., Fernández, M., & González, J. S. (2007) · Animal Feed Science and Technology · doi:10.1016/j.anifeedsci.2007.05.040 · Cited by 42 · see citing works
Self-citationGarcía-González, R., González, J. S., & López, S. (2010) · Journal of Dairy Science · doi:10.3168/jds.2010-3107 · Cited by 39 · see citing works
Self-citationChizzola, R., Hochsteiner, W., & Hajek, S. (2003) · Research in Veterinary Science · doi:10.1016/j.rvsc.2003.07.001 · Cited by 36 · see citing works
Effects of hops on in vitro ruminal fermentation of diets varying in forage content
Narvaez, N., Wang, Y., Xu, Z., et al. (2011) · Livestock Science · doi:10.1016/j.livsci.2010.12.028 · Cited by 32 · see citing works
Ghasemi, S., Naserian, A. A., Valizadeh, Ř., et al. (2011) · Small Ruminant Research · doi:10.1016/j.smallrumres.2011.09.052 · Cited by 31 · see citing works
The ABC Clinical Guide to Herbs
Bauer, B. A. (2003) · Annals of Internal Medicine · doi:10.7326/0003-4819-139-6-200309160-00034 · Cited by 30 · see citing works
Staerfl, S. M., Kreuzer, M., & Soliva, C. R. (2010) · Journal of Animal and Feed Sciences · doi:10.22358/jafs/66338/2010 · Cited by 26 · see citing works
A meta-analysis of malate effects on methanogenesis in ruminal batch cultures
Ungerfeld, E. M., & Forster, R. J. (2011) · Animal Feed Science and Technology · doi:10.1016/j.anifeedsci.2011.04.018 · Cited by 25 · see citing works
Zeleke, A. B., Clément, C., Hess, H. D., et al. (2006) · International Congress Series · doi:10.1016/j.ics.2006.01.017 · Cited by 22 · see citing works
Some Prophylactic Options to Mitigate Methane Emission from Animal Agriculture in Japan
Takahashi, J. (2010) · Asian-Australasian Journal of Animal Sciences · doi:10.5713/ajas.2011.r.03 · Cited by 22 · see citing works
Ebrahimi, S. H., Mohini, M., Singhal, K. K., Miri, V. H., & Tyagi, A. K. (2011) · Archives of Animal Nutrition · doi:10.1080/1745039x.2011.594345 · Cited by 15 · see citing works
Becker, P. M., & Wikselaar, P. G. V. (2011) · Animal Feed Science and Technology · doi:10.1016/j.anifeedsci.2011.09.010 · Cited by 13 · see citing works
Chaves, A. V., Schei, I., Wang, Y., McAllister, T. A., & Benchaar, C. (2009) · Canadian Journal of Animal Science · doi:10.4141/cjas08062 · Cited by 12 · see citing works
Preliminaryin vitrostudy on the effect of xanthohumol on rumen methanogenesis
Zmora, P., Cieślak, A., Jędrejek, D., et al. (2011) · Archives of Animal Nutrition · doi:10.1080/1745039x.2011.644917 · Cited by 11 · see citing works
Medicinal plants as feed additives in animal nutrition.
López, S. A. R. M., García-González, R., López, M., et al. (2007) · Cited by 4 · see citing works
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Critical evaluation of essential oils as rumen modifiers in ruminant nutrition: a review
Cobellis, G., Trabalza-Marinucci, M., & Yu, Z. (2016) · Science of The Total Environment · doi:10.1016/j.scitotenv.2015.12.103 · Cited by 291 · see citing works
Hassan, F.-U., Arshad, M. A., Ebeid, H. M., Rehman, M. S.-U., Khan, M. S., Shahid, S., & Yang, C. (2020) · Frontiers in Veterinary Science · doi:10.3389/fvets.2020.575801 · Cited by 160 · see citing works
New aspects and strategies for methane mitigation from ruminants
Kumar, S., Choudhury, P. K., Carro, M. D., Griffith, G. W., Dagar, S. S., Puniya, M., Calabro, S., Ravella, S. R., Dhewa, T., Upadhyay, R. C., et al. (2014) · Applied Microbiology and Biotechnology · doi:10.1007/s00253-013-5365-0 · Cited by 152 · see citing works
Vargas, J. E., Andrés, S., López-Ferreras, L., Snelling, T. J., Yáñez-Ruíz, D. R., García-Estrada, C., & López, S. (2020) · Scientific Reports · doi:10.1038/s41598-020-58401-z · Cited by 113 · see citing works
Self-citationAdejoro, F. A., Hassen, A., & Akanmu, A. M. (2019) · Animals · doi:10.3390/ani9110863 · Cited by 58 · see citing works
Martínez-Fernández, G., Abecia, L., Martín-García, A. I., Ramos-Morales, E., Hervás, G., Molina-Alcaide, E., & Yáñez-Ruiz, D. R. (2013) · animal · doi:10.1017/s1751731113001699 · Cited by 41 · see citing works
Ramos-Morales, E., de la Fuente, G., Duval, S., Wehrli, C., Bouillon, M., Lahmann, M., Preskett, D., Braganca, R., & Newbold, C. J. (2017) · Frontiers in Microbiology · doi:10.3389/fmicb.2017.00399 · Cited by 41 · see citing works
Garcia, F., Colombatto, D., Brunetti, M. A., Martínez, M. J., Moreno, M. V., Scorcione Turcato, M. C., Lucini, E., Frossasco, G., & Martínez Ferrer, J. (2020) · Animals · doi:10.3390/ani10050786 · Cited by 32 · see citing works
Nawab, A., Li, G., An, L., Nawab, Y., Zhao, Y., Xiao, M., Tang, S., & Sun, C. (2020) · Annals of Animal Science · doi:10.2478/aoas-2020-0005 · Cited by 31 · see citing works
Garcia, F., Vercoe, P. E., Martínez, M. J., Durmic, Z., Brunetti, M. A., Moreno, M. V., Colombatto, D., Lucini, E., & Ferrer, J. M. (2019) · Animal Production Science · doi:10.1071/an17469 · Cited by 14 · see citing works
- Authors
- Bodas, R., Prieto, N., García-González, R., Andrés, S., Giráldez, F. J., & López, S.
- Affiliations
- Instituto de Ganadería de Montaña (ES)
- Universidad de León (ES)
- Corresponding author
- Bodas, R.
- Venue
- Animal Feed Science and Technology
- Publisher
- Elsevier BV
- Published
- 2012-09
- Volume
- 176
- Issue
- 1-4
- Pages
- 78-93
- ISSN
- 0377-8401 (ISSN-L)
- OpenAlex
- W1970303538
- Cited by
- 437
- References
- 179
- Citations by year
- 2026: 19 · 2025: 23 · 2024: 40 · 2023: 37 · 2022: 42 · 2021: 51 · 2020: 40 · 2019: 34 · 2018: 40 · 2017: 28 · 2016: 24 · 2015: 25 · 2014: 17 · 2013: 16
- FWCI
- 37.26
- Type
- journal article
- Language
- en
- Open access
- closed
- Locations
- Animal Feed Science and Technology (publishedVersion)
- DIGITAL.CSIC (Spanish National Research Council (CSIC)) (submittedVersion)
- Funders
- Spanish Ministry of Science and Innovation
- Topics
- Life Sciences › Agricultural and Biological Sciences › Agronomy and Crop Science › Ruminant Nutrition and Digestive Physiology
- Life Sciences › Agricultural and Biological Sciences › Animal Science and Zoology › Animal Nutrition and Physiology
- Physical Sciences › Engineering › Building and Construction › Anaerobic Digestion and Biogas Production
- Keywords
- rumen fermentation, methane production, plant secondary metabolites, ruminant methane mitigation, saponins, tannins, essential oils, rumen microbiota, volatile fatty acids, ammonia nitrogen, rumen protozoa, rumen fungi, rumen bacteria, feed additives, greenhouse gas emissions
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