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Plant components with specific activities against rumen methanogens

Published online by Cambridge University Press:  06 June 2013

A. Cieslak*
Affiliation:
Department of Animal Nutrition and Feed Management, Poznan University of Life Sciences, Wolynska 33, 60-637 Poznan, Poland
M. Szumacher-Strabel
Affiliation:
Department of Animal Nutrition and Feed Management, Poznan University of Life Sciences, Wolynska 33, 60-637 Poznan, Poland
A. Stochmal
Affiliation:
Institute of Soil Science and Plant Cultivation, State Research Institute, Department of Biochemistry and Crop Quality, Czartoryskich 8, 24-100 Pulawy, Poland
W. Oleszek
Affiliation:
Institute of Soil Science and Plant Cultivation, State Research Institute, Department of Biochemistry and Crop Quality, Czartoryskich 8, 24-100 Pulawy, Poland
*
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Abstract

A wide range of plant bioactive components (phytochemicals) have been identified as having potential to modulate the processes of fermentation in the rumen. The use of plants or plant extracts as natural feed additives has become a subject of interest not only among nutritionists but also other scientists. Although a large number of phytochemicals (e.g. saponins, tannins and essential oils) have recently been investigated for their methane reduction potential, there have not yet been major breakthroughs that could be applied in practice. A key tenet of this paper is the need for studies on the influence of plant components on methane production to be performed with standardized samples. Where there are consistent effects, the literature suggests that saponins mitigate methanogenesis mainly by reducing the number of protozoa, condensed tannins both by reducing the number of protozoa and by a direct toxic effect on methanogens, whereas essential oils act mostly by a direct toxic effect on methanogens. However, because the rumen is a complex ecosystem, analysis of the influence of plant components on the populations of methanogens should take into account not only the total population of methanogens but also individual orders or species. Although a number of plants and plant extracts have shown potential in studies in vitro, these effects must be confirmed in vivo.

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Copyright © The Animal Consortium 2013 

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References

Agarwal, N, Shekhar, C, Kumar, R, Chaudhary, LC, Kamra, DN 2009. Effect of peppermint (Mentha piperita) oil on in vitro methanogenesis and fermentation of feed with buffalo rumen liquor. Animal Feed Science and Technology 148, 321327.CrossRefGoogle Scholar
Animut, G, Goetsch, AL, Puchala, R, Patra, AK, Sahlu, T, Varel, VH, Wells, J 2008a. Methane emission by goats consuming diets with different levels of condensed tannins from lespedeza. Animal Feed Science and Technology 144, 212227.Google Scholar
Animut, G, Goetsch, AL, Puchala, R, Patra, AK, Sahlu, T, Varel, VH, Wells, J 2008b. Methane emission by goats consuming different sources of condensed tannins. Animal Feed Science and Technology 144, 228241.Google Scholar
Araujo, RC, Pires, AV, Mourão, GB, Abdallab, AL, Sallam, SMA 2011. Use of blanks to determine in vitro net gas and methane production when using rumen fermentation modifiers. Animal Feed Science and Technology 166167, 155–162.Google Scholar
Beauchemin, KA, McGinn, SM, Martinez, TF, McAllister, TA 2007. Use of condensed tannin extract from quebracho trees to reduce methane emissions. Journal of Animal Science 85, 19901996.Google Scholar
Bhatta, R, Baruah, L, Saravanan, M, Suresh, KP, Sampath, KT 2012. Effect of medicinal and aromatic plants on rumen fermentation, protozoa population and methanogenesis in vitro. Journal of Animal Physiology and Animal Nutrition, doi: 10.1111/j.1439-0396.2012.01285.x.Google Scholar
Bhatta, R, Uyeno, Y, Tajima, K, Takenaka, A, Yabumoto, Y, Nonaka, I, Enishi, O, Kurihara, M 2009. 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 92, 55125522.CrossRefGoogle ScholarPubMed
Bodas, RN, Prieto, NR, García-González, RS, Andrés, S, Giráldez, FJ, López, S 2012. Manipulation of rumen fermentation and methane production with plant secondary metabolites. Animal Feed Science and Technology 176, 7893.Google Scholar
Busquet, M, Calsamiglia, S, Ferret, A, Carro, MD, Kamel, C 2005. Effect of garlic oil and four of its compounds on rumen microbial fermentation. Journal of Dairy Science 88, 43934404.Google Scholar
Calsamiglia, S, Busquet, M, Cardozo, PW, Castillejos, L, Ferret, A 2007. Invited review: essential oils as modifiers of rumen microbial fermentation. Journal of Dairy Science 90, 25802595.Google Scholar
Carulla, JE, Kreuzer, M, Machmueller, A, Hess, HD 2005. Supplementation of Acacia mearnsii tannins decreases methanogenesis and urinary nitrogen in forage fed sheep. Australian Journal of Agricultural Research 56, 961970.Google Scholar
Chaves, AV, Baah, J, Wang, Y, McAllister, TA, Benchaar, Ch 2012. Effects of cinnamon leaf, oregano and sweet orange essential oils on fermentation and aerobic stability of barley silage. Journal of the Science of Food and Agriculture 92, 906915.Google Scholar
Cheeke, PR 1996. Biological effects of feed and forage saponins and their impact on animal production. Advanced Experimental Medicine Biology 405, 377385.CrossRefGoogle ScholarPubMed
Cieslak, A, Váradyová, Z, Kišidayová, S, Szumacher-Strabel, M 2009a. The effects of linoleic acid on the fermentation parameters, population density, and fatty-acid profile of two rumen ciliate cultures, Entodinium caudatum and Diploplastron affine. Acta Protozoologica 48, 5161.Google Scholar
Cieslak, A, Zmora, P, Nowakowska, A, Szumacher-Strabel, M 2009b. Limonene affect rumen methanogenesis inhibiting the methanogens population. Bioactive plant compounds – structural and applicative aspects. Acta Biochimica Polonica 56, 5961.Google Scholar
Cieslak, A, Zmora, P, Pers-Kamczyc, E, Szumacher-Strabel, M 2012. Effects of tannins source (Vaccinium vitis idaea L.) on rumen microbial fermentation in vivo. Animal Feed Sciences and Technology 176, 102106.Google Scholar
Cieslak, A, Miltko, R, Belzecki, G, Szumacher-Strabel, M, Potkanki, A, Kwiatkowska, E, Michalowski, T 2006. Effect of vegetable oils on the methane concentration and population density of the rumen ciliate, Eremoplastron dilobum, grown in vitro. Journal of Animal and Feed Sciences 15, 1518.Google Scholar
Demeyer, DI, De Graeve, K 1991. Differences in stoichiometry between rumen and hindgut fermentation. Journal of Animal Physiology and Animal Nutrition 22, 5061.Google Scholar
Dorman, HJ, Deans, SG 2000. Antimicrobial agents from plants: antibacterial activity of plant volatile oils. Journal of Applied Microbiology 88, 308316.Google Scholar
Duffy, CF, Killeen, GF, Connolly, CA, Power, RF 2001. Effects of dietary supplementation with Yucca schidigera Roezl ex Ortgies and its saponin and non-saponin fractions on rat metabolism. Journal of Agricultural Food Chemistry 49, 34083413.Google Scholar
Evans, JD, Martin, SA 2000. Effects of thymol on ruminal micro-organisms. Current Microbiology 41, 336340.Google Scholar
Finlay, BJ, Esteban, G, Clarke, KJ, Williams, AG, Embley, TM, Hirt, RR 1994. Some rumen ciliates have endosymbiotic methanogens. FEMS Microbiology Letters 117, 157161.Google Scholar
Goel, G, Makkar, HPS 2012. Methane mitigation from ruminants using tannins and saponins. Tropical Animal Health Production 44, 729739.CrossRefGoogle ScholarPubMed
Goel, G, Makkar, HPS, Becker, K 2008. Changes in microbial population, methanogenesis and rumen fermentation in response to saponin rich fractions of different plant materials. Journal of Applied Microbiology 105, 770777.Google Scholar
Goel, G, Makkar, HPS, Becker, K 2009. Inhibition of methanogens by bromochloromethane: effects on microbial communities and rumen fermentation using batch and continuous fermentations. The British Journal of Nutrition 101, 14841492.Google Scholar
Grainger, C, Clarke, T, Auldist, MJ, Beauchemin, KA, McGinn, SM, Waghorn, GC, Eckard, RJ 2009. Potential use of Acacia mearnsii condensed tannins to reduce methane emissions and nitrogen excretion from grazing dairy cows. Canadian Journal of Animal Science 89, 241251.Google Scholar
Guo, YQ, Liu, JX, Lu, Y, Zhu, WY, Denman, SE, McSweeney, CS 2008. Effect of tea saponin on methanogenesis, microbial community structure and expression of mcrA gene, in cultures of rumen microorganisms. Letters Applied Microbiology 47, 421426.Google Scholar
Hariadi, BT, Santoso, B 2010. Evaluation of tropical plants containing tannin on in vitro methanogenesis and fermentation parameters using rumen fluid. Journal of the Science of Food and Agriculture 90, 456461.CrossRefGoogle ScholarPubMed
Hassanat, F, Benchaar, C 2013. 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 Science of Food and Agriculture 93, 332339.Google Scholar
Hess, HD, Kreuzer, M, Diaz, TE, Lascano, CE, Carulla, JE, Soliva, CR, Machműller, A 2003. Saponin rich tropical fruits affect fermentation and methanogenesis in faunated and defaunated rumen fluid. Animal Feed Science and Technology 109, 7994.Google Scholar
Holtshausen, L, Chaves, AV, Beauchemin, KA, McGinn, SM, McAllister, TA, Odongo, NE, Cheeke, PR, Benchaar, C 2009. Feeding saponin-containing Yucca schidigera and Quillaja saponaria to decrease enteric methane production in dairy cows. Journal of Dairy Science 92, 28092821.Google Scholar
Hook, SE, Wright, AD, McBride, BW 2010. Methanogens: methane producers of the rumen and mitigation strategies. Archaea, Article ID: 945785, doi: 10.1155/2010/945785.Google Scholar
Hu, WL, Liu, JX, Ye, JA, Wu, YM, Guo, YQ 2005. Effect of tea saponin on rumen fermentation in vitro. Animal Feed Science and Technology 120, 333339.Google Scholar
Huang, XD, Tan, HY, Long, R, Liang, JB, Wright, AD 2012. Comparison of methanogen diversity of yak (Bos grunniens) and cattle (Bos taurus) from the Qinghai-Tibetan plateau, China. BMC Microbiology 12, 237247.Google Scholar
Hungate, RE 1967. Hydrogen as an intermediate in the rumen fermentation. Archives of Microbiology 40, 952958.Google Scholar
Hungate, RE, Smith, W, Bauchop, T 1970. Formate as an intermediate in the rumen fermentation. Journal of Bacteriology 102, 389397.Google Scholar
Janssen, PH, Kirs, M 2008. Structure of the archaeal community of the rumen. Applied and Environmental Microbiology 74, 36193625.Google Scholar
Jarvis, GN, Strompl, C, Burgess, DM, Skillman, LC, Moore, ER, Joblin, KN 2000. Isolation and identification of ruminal methanogens from grazing cattle. Current Microbiology 40, 327332.Google Scholar
Jayanegara, A, Leiber, F, Kreuzer, M 2012. Meta-analysis of the relationship between dietary tannin level and methane formation in ruminants from in vivo and in vitro experiments. Journal of Animal Physiology and Animal Nutrition 96, 365375.Google Scholar
Jouany, JP, Morgavi, DP 2007. Use of ‘natural’ products as alternatives to antibiotic feed additives in ruminant production. Animal 1, 14431466.Google Scholar
Kamra, DN 2005. Rumen microbial ecosystem. Current Science 89, 124132.Google Scholar
Kaneda, N, Nakanishi, H, Staba, J 1987. Steroidal constituents of Yucca schidigera plants and tissue cultures. Phytochemistry 26, 14251429.Google Scholar
King, EE, Smith, RP, St-Pierre, B, Wright, AD 2011. Differences in the rumen methanogen populations of lactating Jersey and Holstein dairy cows under the same diet regimen. Applied and Environmental Microbiology 77, 56825687.Google Scholar
Kisidayova, S, Varyadova, Z, Zelenak, I, Siroka, P 2000. Methanogenesis in rumen ciliate cultures of Entodinium caudatum and Epidinium ecaudatum after long-term cultivation in a chemically defined medium. Folia Microbiologica 45, 269274.Google Scholar
Kongmun, P, Wanapat, M, Pakdee, P, Navanukraw, C, Yu, Z 2011. Manipulation of rumen fermentation and ecology of swamp buffalo by coconut oil and garlic powder supplementation. Livestock Science 135, 8492.Google Scholar
Kowalczyk, M, Pecio, L, Stochmal, A, Oleszek, W 2011. Qualitative and quantitative analysis of steroidal saponins in crude extract and bark powder of Yucca schidigera Roezl. Journal of Agricultural Food Chemistry 59, 80588064.Google Scholar
Kumar, S, Dagar, SS, Puniya, AK, Upadhyay, RC 2013. Changes in methane emission, rumen fermentation in response to diet and microbial interactions. Research in Veterinary Science 94, 263268.Google Scholar
Leahy, SC, Kelly, WJ, Altermann, E, Ronimus, RS, Yeoman, CJ, Pacheco, DM, Li, D, Kong, Z, McTavish, S, Sang, C, Lambie, SC, Janssen, PH, Dey, D, Attwood, GT 2010. The genome sequence of the rumen methanogen Methanobrevibacter ruminantium reveals new possibilities for controlling ruminant methane emissions. PLoS One 5, e8926. doi:10.1371/journal.pone.0008926.Google Scholar
Lee, J-H, Rhee, M-S, Kumar, S, Lee, G-H, Chang, D-H, Kim, D-S, Choi, S-H, Lee, D-W, Yoon, M-H, Kim, B-C 2013. Genome sequence of Methanobrevibacter sp. strain JH1, isolated from rumen of Korean native cattle. Genome Announcements 1, e00002-13. doi:10.1128/genomeA.00002-13.Google Scholar
Li, W, Powers, W 2012. Effects of saponin extracts on air emissions from steers. Journal of Animal Science 90, 40014013.Google Scholar
Lin, B, Lu, Y, Wang, JH, Liang, Q, Liu, JX 2012a. The effects of combined essential oils along with fumarate on rumen fermentation and methane production in vitro. Journal of Animal and Feed Sciences 21, 198210.Google Scholar
Lin, B, Wang, JH, Lu, Y, Liang, Q, Liu, JX 2012b. In vitro rumen fermentation and methane production are influenced by active components of essential oils combined with fumarate. Journal of Animal Physiology and Animal Nutrition 97, 19.Google Scholar
Macheboeuf, D, Morgavi, DP, Papon, Y, Mousset, JL, Arturo-Schaan, M 2008. Dose–response effects of essential oils on in vitro fermentation activity of the rumen microbial population. Animal Feed Science and Technology 145, 335350.Google Scholar
Makkar, HPS, Becker, K 1997. Degradation of Quillaja saponins by mixed culture of rumen microbes. Letters Applied Microbiology 25, 243245.Google Scholar
Manh, NS, Wanapat, M, Uriyapongson, S, Khejornsart, P, Chanthakhoun, V 2012. Effect of eucalyptus (Camaldulensis) leaf meal powder on rumen fermentation characteristics in cattle fed on rice straw. African Journal of Agricultural Research 7, 19972003.Google Scholar
Mao, HL, Wang, JK, Zhou, YY, Liu, JX 2010. Effects of addition of tea saponins and soyabean oil on methane production, fermentation and microbial population in the rumen of growing lambs. Livestock Science 129, 5662.Google Scholar
McIntosh, FM, Williams, P, Losa, R, Wallace, RJ, Beever, DA, Newbold, CJ 2003. Effects of essential oils on ruminal microorganism and their protein metabolism. Applied and Environmental Microbiology 69, 50115014.Google Scholar
Miles, CO, Wilkins, AL, Munday, SC, Holland, PT, Smith, BL, Lancaster, MJ, Embling, PP 1992. Identification of the calcium salt of epismilagenin beta-d-glucuronide in the bile crystals of sheep affected by Panicum-dichotomiflorum and Panicum-schinzii toxicoses. Journal of Agricultural Food Chemistry 40, 16061609.Google Scholar
Morgavi, DP, Forano, E, Martin, C, Newbold, CJ 2010. Microbial ecosystem and methanogenesis in ruminants. Animal 4, 10241036.Google Scholar
Morgavi, DP, Martin, C, Jouany, JP, Ranilla, MJ 2012. Rumen protozoa and methanogenesis: not a simple cause–effect relationship. The British Journal of Nutrition 107, 388397.Google Scholar
Morvan, B, Bonnemoy, F, Fonty, G, Gouet, P 1996. Quantitative determination of H2-utilizing acetogenic and sulfate-reducing bacteria and methanogenic archaea from digestive track of different mammals. Current Microbiology 32, 129133.Google Scholar
Morvan, B, Dore, J, Rieulesme, F, Foucat, L, Fonty, G, Gouet, P 1994. Establishment of hydrogen-utilizing bacteria in the rumen of the newborn lamb. FEMS Microbiology Letters 117, 249256.Google Scholar
Narvaez, N, Wang, Y, McAllister, T 2013. Effects of extracts of Humulus lupulus (hops) and Yucca schidigera applied alone or in combination with monensin on rumen fermentation and microbial populations in vitro. Journal of Science of Food and Agriculture, doi: 10.1002/jsfa.6068.Google Scholar
Newbold, CJ, Lassalas, B, Jouany, JP 1995. The importance of methanogens associated with ciliate protozoa in ruminal methane production in vitro. Letters in Applied Microbiology 21, 230234.Google Scholar
Newbold, CJ, ElHassan, SM, Wang, J, Ortega, ME, Wallace, RJ 1997. Influence of foliage from African multipurpose trees on activity of rumen protozoa and bacteria. The British Journal of Nutrition 78, 237249.Google Scholar
Niderkorn, V, Baumont, R, Le Morvan, A, Macheboeuf, D 2011. Occurrence of associative effects between grasses and legumes in binary mixtures on in vitro rumen fermentation characteristics. Journal of Animal Science 89, 11381145.Google Scholar
O'Ghara, EA, Hill, DJ, Maslin, DJ 2000. Activities of garlic oil, garlic powder, and their diallyl constituents against Helicobacter pylori. Applied and Environmental Microbiology 66, 22692273.CrossRefGoogle Scholar
Odenyo, AA, Osuji, PO, Karanfil, O 1997. Effect of multipurpose tree (MPT) supplements on ruminal ciliate protozoa. Animal Feed Science and Technology 67, 169180.Google Scholar
Ohene-Adjei, S, Teather, RM, Ivan, M, Forster, RJ 2007. Postinoculation protozoan establishment and association patterns of methanogenic Archaea in the ovine rumen. Applied and Environmental Microbiology 73, 46094618.Google Scholar
Ohene-Adjei, S, Chaves, AV, McAllister, TA, Benchaar, TA, Teather, C, Forster, RJ 2008. Evidence of increased diversity of methanogenic archea with plant extract supplementation. Microbial Ecology 56, 234242.Google Scholar
Oleszek, W, Sitek, M, Stochmal, A, Piacente, S, Pizza, C, Cheeke, P 2001. Steroidal saponins of Yucca schidigera Roezl. Journal of Agricultural Food Chemistry 49, 43924396.Google Scholar
Patra, AK, Saxena, J 2009. Dietary phytochemicals as rumen modifiers: a review of the effects on microbial populations. Antonie van Leeuwenhoek 96, 369375.Google Scholar
Patra, AK, Saxena, J 2010. A new perspective on the use of plant secondary metabolites to inhibit methanogenesis in the rumen. Phytochemistry 71, 11981222.Google Scholar
Patra, AK, Yu, Z 2012. Effects of essential oils on methane production and fermentation by, and abundance and diversity of, rumen microbial populations. Applied and Environmental Microbiology 78, 42714280.Google Scholar
Patra, AK, Kamra, DN, Agarwal, N 2010. Effects of extracts of spices on rumen methanogenesis, enzyme activities and fermentation of feeds in vitro. Journal of the Science of Food and Agriculture 90, 511520.Google Scholar
Pellikaan, WF, Stringano, E, Leenaars, J, Bongers, DJGM, van Laar-van Schuppen, S, Plant, J, Mueller-Harvey, I 2011. Evaluating effects of tannins on extent and rate of in vitro gas and CH4 production using an automated pressure evaluation system (APES). Animal Feed Science and Technology 166167, 377–390.Google Scholar
Pen, B, Sar, C, Mwenya, B, Takahashi, J 2008. Effects of Quillaja saponaria extract alone or in combination with Yucca schidigera extract on ruminal fermentation and methanogenesis in vitro. Animal Science Journal 79, 193199.Google Scholar
Pen, B, Takaura, K, Yamaguchi, S, Asa, R, Takahashi, J 2007. Effects of Yucca schidigera and Quillaja saponaria with or without b-1, 4 galactooligosaccharides on ruminal fermentation, methane production and nitrogen utilization in sheep. Animal Feed Science and Technology 138, 7588.Google Scholar
Pen, B, Sar, C, Mwenya, B, Kuwaki, K, Morikawa, R, Takahashi, J 2006. Effects of Yucca schidigera and Quillaja saponaria extracts on in vitro ruminal fermentation and methane emission. Animal Feed Science and Technology 129, 175186.Google Scholar
Pers-Kamczyc, E, Zmora, P, Cieslak, A, Szumacher-Strabel, M 2011. Development of nucleic acid based techniques and possibilities of their application to rumen microbial ecology research. Journal of Animal and Feed Sciences 20, 315337.Google Scholar
Popova, M, Morgavi, DP, Martin, C 2012. Methanogens and methanogenesis in the rumen and cecum of lambs fed two different high-concentrate diets. Applied and Environmental Microbiology doi:10.1128/AEM.03115-12.Google Scholar
Ramirez-Restrepo, CA, Barry, TN, Marriner, A, Lopez-Villalobos, N, McWilliam, EL, Lassey, KR, Clark, H 2010. Effects of grazing willow fodder blocks upon methane production and blood composition in young sheep. Animal Feed Science and Technology 155, 3343.Google Scholar
Ranilla, MJ, Morgavi, DP, Jouany, JP 2004. Effect of time after defaunation on methane production in vitro. Reproduction Nutrition Development 44, S35S36.Google Scholar
Regensbogenova, M, Kisidayova, S, Michalowski, T, Javorsky, P, Moon-Van Der Staay, GWM, Moon-Van Der Staay, SY, Hackstein, JHP, McEwan, NR, Jouany, JP, Newbold, JC, Pristas, P 2004. Rapid identification of rumen protozoa by restriction analysis of amplified 18S rRNA gene. Acta Protozoologica 43, 219224.Google Scholar
Russell, MJ, Hall, AJ, Cairns-Smith, AG, Braterman, PS 1988. Submarine hot springs and the origin of life. Nature 336, 117117.Google Scholar
Sallam, SMA, Abdelgaleil, SAM 2010. Effect of different levels of citrus essential oil and its active components on rumen microbial fermentation and methane emission in vitro. Cuban Journal of Agriculture Science 44, 367371.Google Scholar
Sallam, SMA, Bueno, ICS, Brigide, P, Godoy, PB, Vitti, DMSS, Abdalla, AL 2009. Efficacy of eucalyptus oil on in vitro rumen fermentation and methane production. Options Mediterraneennes 85, 267272.Google Scholar
Sallam, SMA, Abdelgaleil, SAM, Bueno, ICDS, Nasser, MEA, Araujo, R, Abdalla, AL 2011. Effect of some essential oils on in vitro methane emission. Archives of Animal Nutrition 65, 203214.Google Scholar
Shin, EC, Choi, BR, Lim, WJ, Hong, SY, An, CL, Cho, KM, Kim, YK, An, JM, Kang, JM, Lee, SS, Kim, H, Yun, HD 2004. Phylogenetic analysis of archaea in three fractions of cow rumen based on the 16S rDNA sequence. Anaerobe 10, 313319.Google Scholar
Skillman, LC, Evans, PN, Naylor, GE, Morvan, B, Jarvis, GN, Joblin, KN 2004. 16S ribosomal DNA-directed PCR primers for ruminal methanogens and identification of methanogens colonising young lambs. Anaerobe 10, 277285.Google Scholar
Smith, AH, Zoetendal, EG, Mackie, RI 2005. Bacterial mechanisms to overcome inhibitory effects of dietary tannins. Microbial Ecology 50, 197205.Google Scholar
Soliva, CR, Widmer, S, Kreuzer, M 2008. Ruminal fermentation of mixed diets supplemented with St. John's Wort (Hypericum perforatum) flowers and pine (Pinus mugo) oil or mixtures containing these preparations. Journal of Animal and Feed Sciences 17, 352362.Google Scholar
Soltan, YA, Morsy, AS, Sallam, SMA, Louvandini, H, Abdalla, AL 2012. Comparative in vitro evaluation of forage legumes (prosopis, acacia, atriplex, and leucaena) on ruminal fermentation and methanogenesis. Journal of Animal and Feed Sciences 21, 759772.Google Scholar
Staerfl, SM, Kreuzer, M, Soliva, CR 2010. In vitro screening of unconventional feeds and various natural supplements for their ruminal methane mitigation potential when included in a maize-silage based diet. Journal of Animal and Feed Sciences 19, 651664.Google Scholar
Stewart, CS, Flint, HJ, Bryant, MP 1997. The rumen bacteria. In The rumen microbial ecosystem (ed. PN Hobson and CS Stewart), pp. 1072. Blackie Academic and Professional, London, UK.Google Scholar
St-Pierre, B, Wright, AD 2012. Diversity of gut methanogens in herbivorous animals. Animal 7 (suppl. 1), 4956.Google Scholar
Szumacher-Strabel, M, Cieslak, A 2010. Potential of phytofactors to mitigate rumen ammonia and methane production. Journal of Animal and Feed Sciences 19, 319337.Google Scholar
Szumacher-Strabel, M, Cieslak, A, Nowakowska, A 2009. Effect of oils rich in linoleic acid on in vitro rumen fermentation parameters of sheep, goats and dairy cows. Journal of Animal and Feed Sciences 18, 440452.Google Scholar
Szumacher-Strabel, M, Zmora, P, Roj, E, Stochmal, A, Pers-Kamczyc, E, Urbanczyk, A, Oleszek, W, Lechniak, D, Cieslak, A 2011. In vitro screening of the wild dog rose (Rosa canina) potential to mitigate rumen methane production. Journal of Animal and Feed Sciences 20, 285299.Google Scholar
Tajima, K, Nagamine, T, Matsui, H, Nakamura, M, Animov, RI 2001. Phylogenetic analysis of archaeal 16S rRNA libraries from the rumen suggests the existence of a novel group of archaea not associated with known methanogens. FEMS Microbiology Letters 200, 6772.Google Scholar
Tan, HY, Sieo, CC, Abdullah, N, Liang, JB, Huang, XD, Ho, YW 2011. Effects of condensed tannins from Leucaena on methane production, rumen fermentation and populations of methanogens and protozoa in vitro. Animal Feed Science and Technology 169, 185193.Google Scholar
Tanaka, O, Ikeda, T, Ohtani, K, Kasai, R, Yamasaki, K 2000. Antiyeast steroidal saponins from Yucca schidigera (Mohave Yucca), a new anti-food-deteriorating agent. Journal of Natural Products 63, 332338.Google Scholar
Tavendale, MH, Meagher, LP, Pacheco, D, Walker, N, Attwood, GT, Sivakumaran, S 2005. Methane production from in vitro rumen incubations with Lotus pedunculatus and Medicago sativa, and effects of extractable condensed tannin fractions on methanogenesis. Animal Feed Science and Technology 123–124, 403419.Google Scholar
Teferedegne, B, McIntosh, F, Osuji, PO, Odenyo, A, Wallace, RJ, Newbold, CJ 1999. Influence of foliage from different accessions of the sub-tropical leguminous tree, Sesbania sesban, on ruminal protozoa in Ethiopian and Scottish sheep. Animal Feed Science and Technology 78, 1120.Google Scholar
Tymensen, LD, Beauchemin, KA, McAllister, TA 2012. Structures of free-living and protozoa-associated methanogen communities in the bovine rumen differ according to comparative analysis of 16S rRNA and mcrA genes. Microbiology 158, 18081817.Google Scholar
Ushida, K, Jouany, JP 1996. Methane production associated with rumen-ciliated protozoa and its effect on protozoan activity. Letters in Applied Microbiology 23, 129132.Google Scholar
Van Kessel, JS, Russell, JB 1996. The effect of pH on ruminal methanogenesis. FEMS Microbiology Ecology 20, 205210.Google Scholar
Vasta, V, Bessa, RJB 2012. Manipulating ruminal biohydrogenation by the use of plants bioactive compounds. In Dietary phytochemicals and microbes (ed. AK Patra), pp. 263284. Springer, London, UK.Google Scholar
Vogels, GD, Hoppe, WF, Stumm, CK 1980. Association of methanogenic bacteria with rumen ciliates. Applied and Environmental Microbiology 47, 219221.Google Scholar
Wang, CJ, Wang, SP, Zhou, H 2009. Influences of flavomycin, ropadiar, and saponin on nutrient digestibility, rumen fermentation, and methane emission from sheep. Animal Feed Science and Technology 148, 157166.Google Scholar
Wang, XF, Mao, SY, Liu, JH, Zhang, LL, Cheng, YF, Jin, W, Zhu, WY 2011. Effect of the gynosaponin on methane production and microbe numbers in a fungus-methanogen co-culture. Journal of Animal and Feed Sciences 20, 272284.Google Scholar
Wang, Y, McAllister, TA, Newbold, CJ, Rode, LM, Cheeke, PR, Cheng, KJ 1998. Effects of Yucca schidigera extract on fermentation and degradation of steroidal saponins in the rumen simulation technique (RUSITEC). Animal Feed Science and Technology 74, 143153.Google Scholar
Whitmann, WB, Bowen, TL, Boone, DR 1992. The methanogenic bacteria. In The prokaryotes, 2nd ed. A handbook on the biology of bacteria: ecophysiology, isolation, identification, applications (ed. A Balows), pp. 719767. Springer-Verlag, New York, USA.Google Scholar
Wina, E, Muetzel, S, Hoffmann, E, Makkar, HPS, Becker, K 2005. Saponins containing methanol extract of Sapindus rarak affect microbial fermentation, microbial activity and microbial community structure in vitro. Animal Feed Science and Technology 121, 159174.Google Scholar
Wolin, MJ, Miller, TL 1988. Microbe–microbe interactions. In The rumen microbial ecosystem (ed. PN Hobson), pp. 343359. Elsevier Science Publishers, New York, USA.Google Scholar
Wolin, MJ, Miller, C, Stewart, CJ 1997. Microbe–microbe interactions. In The rumen microbial ecosystem (ed. PN Hobson and CS Stewart), pp. 467491. London Blackie Academic and Professional, UK.Google Scholar
Wright, ADG, Ma, X, Obispo, NE 2008. Methanobrevibacter phylotypes are the dominant methanogens in sheep from Venezuela. Microbial Ecology 56, 390394.CrossRefGoogle ScholarPubMed
Zeleke, AB, Clement, C, Hess, HD, Kreuzer, M, Soliva, CR 2006. Effect of foliage from multi-purpose trees and a leguminous crop residue on in vitro methanogenesis and ruminal N use. International Congress Series 1293, 168171.Google Scholar
Zhou, M, Hernandez-Sanabria, E, Guan, LL 2009. Assessment of the microbial ecology of ruminal methanogens in cattle with different feed efficiencies. Applied and Environmental Microbiology 75, 65246533.Google Scholar
Zhou, YY, Mao, HL, Jiang, F, Wang, JK, Liu, JX, McSweeney, CS 2011. Inhibition of rumen methanogenesis by tea saponins with reference to fermentation pattern and microbial communities in Hu sheep. Animal Feed Science and Technology 166, 93100.Google Scholar
Zhu, WY, Mao, SY, Liu, JX, Cheng, YF, Iqbal, MF, Wang, JK 2007. Diversity of methanogens and their interactions with other microorganisms in methanogenesis in the rumen. The Proceedings of the VII International Symposium on the Nutrition of Herbivores (ed. QX Meng), pp. 17–22. China Agricultural University Press, Beijing, China.Google Scholar
Zmora, P, Cieslak, A, Pers-Kamczyc, E, Nowak, A, Szczechowiak, J, Szumacher-Strabel, M 2012b. Effects of Mentha piperita L. on in vitro rumen methanogenesis and fermentation. Acta Agriculturae Scandinavica, Section A – Animal Science 62, 4652.Google Scholar
Zmora, P, Cieslak, A, Pers-Kamczyc, E, Szumacher-Strabel, M 2012c. The in vitro study on the effect of Salvia officinalis L. on rumen fermentation. Journal of Animal and Feed Sciences 21, 613623.Google Scholar
Zmora, P, Cieslak, A, Jedrejek, D, Stochmal, A, Pers-Kamczyc, E, Oleszek, W, Nowak, A, Szczechowiak, J, Lechniak, D, Szumacher-Strabel, M 2012a. Preliminary in vitro study on the effect of xanthohumol on rumen methanogenesis. Archives of Animal Nutrition 66, 6671.Google Scholar