Hostname: page-component-78c5997874-ndw9j Total loading time: 0 Render date: 2024-11-12T22:22:41.075Z Has data issue: false hasContentIssue false
  • English
  • Français

Advances in microbial ecosystem concepts and their consequences for ruminant agriculture

Published online by Cambridge University Press:  15 April 2008

J. E. Edwards ,
S. A. Huws ,
E. J. Kim ,
M. R. F. Lee ,
A. H. Kingston-Smith  and
N. D. Scollan
J. E. Edwards*
Affiliation:
Institute of Grassland & Environmental Research, Plas Gogerddan, Aberystwyth, Ceredigion, Wales SY23 3EB, UK
S. A. Huws
Affiliation:
Institute of Grassland & Environmental Research, Plas Gogerddan, Aberystwyth, Ceredigion, Wales SY23 3EB, UK
E. J. Kim
Affiliation:
Institute of Grassland & Environmental Research, Plas Gogerddan, Aberystwyth, Ceredigion, Wales SY23 3EB, UK
M. R. F. Lee
Affiliation:
Institute of Grassland & Environmental Research, Plas Gogerddan, Aberystwyth, Ceredigion, Wales SY23 3EB, UK
A. H. Kingston-Smith
Affiliation:
Institute of Grassland & Environmental Research, Plas Gogerddan, Aberystwyth, Ceredigion, Wales SY23 3EB, UK
N. D. Scollan
Affiliation:
Institute of Grassland & Environmental Research, Plas Gogerddan, Aberystwyth, Ceredigion, Wales SY23 3EB, UK
*
E-mail: [email protected]
Get access

Abstract

Microbial transformations in the rumen ecosystem have a major impact on our ability to meet the challenge of reducing the environmental footprint of ruminant livestock agriculture, as well as enhancing product quality. Current understanding of the rumen microbial ecosystem is limited, and affects our ability to manipulate rumen output. The view of ruminal fermentation as the sum of activities of the dominant rumen microbiota is no longer adequate, with a more holistic approach required. This paper reviews rumen functionality in the context of the microbiota of the rumen ecosystem, addressing ruminal fermentation as the product of an ecosystem while highlighting the consequences of this for ruminant agriculture. Microbial diversity in the rumen ecosystem enhances the resistance of the network of metabolic pathways present, as well as increasing the potential number of new pathways available. The resulting stability of rumen function is further promoted by the existence of rumen microbiota within biofilms. These protected, structured communities offer potential advantages, but very little is currently known about how ruminal microorganisms interact on feed-surfaces and how these communities develop. The temporal and spatial development of biofilms is strongly linked to the availability of dietary nutrients, the dynamics of which must also be given consideration, particularly in fresh-forage-based production systems. Nutrient dynamics, however, impact not only on pathway inputs but also the turnover and output of the whole ecosystem. Knowledge of the optimal balance of metabolic processes and the corresponding microbial taxa required to provide a stable, balanced ecosystem will enable a more holistic understanding of the rumen. Future studies should aim to identify key ecosystem processes and components within the rumen, including microbial taxa, metabolites and plant-based traits amenable to breeding-based modification. As well as gaining valuable insights into the biology of the rumen ecosystem, this will deliver realistic and appropriate novel targets for beneficial manipulation of rumen function.

Keywords

ecosystemmetabolismmicrobiotanutrientrumen
Type
Full Paper
Information
animal , Volume 2 , Issue 5 , May 2008 , pp. 653 - 660
Copyright
Copyright © The Animal Consortium 2008

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

References

Albrecht, KA, Broderick, GA 1992. Ruminal in vitro degradation of protein from different legume species. US Dairy Forage Research Centre, Madison, USA. Research Summaries, pp. 92–94.Google Scholar
Allison, DG, McBain, AJ, Gilbert, P 2000. Biofilms: problems of control. In Community structure and co-operation in biofilms (ed. DG Allison, P Gilbert, HM Lappin-Scott and M Wilson). Cambridge University Press, Cambridge, UK.CrossRefGoogle Scholar
Bartram CJ 1987. The endogenous protein content of ruminant proximal duodenal digests. PhD Thesis, University of Nottingham, Sutton Bonington, Leicestershire, UK.Google Scholar
Beever, DE, Siddons, RC 1986. Digestion and metabolism in the grazing ruminant. In Control of digestion and metabolism in the ruminant (ed. IW McDonald and ACI Warner), pp. 432–447. University of New England Publishing Unit, Armidale, Australia.Google Scholar
Bonhomme, A 1990. Rumen ciliates: their metabolism and relationships with bacteria and their hosts. Animal Feed Science and Technology 30, 203–212.CrossRefGoogle Scholar
Boudon, A, Peyraud, JL 2001. The release of intracellular constituents from fresh ryegrass (Lolium perenne) during ingestive mastication in dairy cows: effect of intracellular constituent, season and stage of maturity. Animal Feed Science and Technology 93, 229–245.CrossRefGoogle Scholar
Bowman, JGP, Firkins, JL 1993. Effects of forage species and particle size on bacterial cellulolytic activity and colonisation in situ. Journal of Animal Science 71, 1623–1633.CrossRefGoogle ScholarPubMed
Broudiscou, L, Jouany, JP 1995. Reassessing the manipulation of protein synthesis by rumen microbes. Reproduction, Nutrition, Development 35, 517–535.CrossRefGoogle ScholarPubMed
Buanafina, MM, de O Langdon, T, Hauck, BD, Dalton, SJ, Morris, P 2006. Manipulating the phenolic acid content and digestibility of Italian ryegrass (Lolium multiflorum) by vacuolar targeted expression of a fungal ferulic acid esterase. Applied Biochemistry and Biotechnology 130, 415–426.CrossRefGoogle Scholar
Buchanan, M 2002. Nexus: small worlds and the groundbreaking science of networks. W. W. Norton & Company Ltd., London, UK.Google Scholar
Cheng, KJ, Fay, JP, Howarth, RE, Costerton, JW 1980. Sequence of events in the digestion of fresh legume leaves by rumen bacteria. Applied and Environmental Microbiology 40, 613–625.CrossRefGoogle ScholarPubMed
Cheng, KJ, McAllister, TA, Costerton, JW 1995. Biofilm of the ruminant digestive tract. In Microbial biofilms (ed. H Lappin-Scott and JM Costerton), pp. 221–232. Cambridge University Press, Cambridge, UK.CrossRefGoogle Scholar
Cho, SJ, Cho, KM, Shin, EC, Lim, WJ, Hong, SY, Choil, BR, Kang, JM, Lee, SM, Kim, YH, Kim, H, Yun, HD 2006. 16S rDNA analysis of bacterial diversity in three fractions of cow rumen. Journal of Microbiology and Biotechnology 16, 92–101.Google Scholar
Christensen, RA, Cameron, MR, Klusmeyer, TH, Elliot, JP, Clark, JH, Nelson, DR, Yu, Y 1993. Influence of the amount and degradability of dietary protein on nitrogen utilization by dairy cows. Journal of Dairy Science 76, 3497–3513.CrossRefGoogle ScholarPubMed
Coe, ML, Nagaraja, TG, Sun, YD, Wallace, N, Towne, EG, Kemp, KE, Hutcheson, JP 1999. Effect of virginiamycin on ruminal fermentation in cattle during adaptation to a high concentrate diet and during an induced acidosis. Journal of Animal Science 77, 2259–2268.CrossRefGoogle ScholarPubMed
Cohen, R, Erez, K, ben-Avraham, D, Havlin, S 2000. Resilience of the internet to random breakdowns. Physical Review Letters 85, 4626–4628.CrossRefGoogle ScholarPubMed
Connon, SA, Giovannoni, SJ 2002. High-throughput methods for culturing microorganisms in very-low nutrient media yield diverse new marine isolates. Applied and Environmental Microbiology 68, 3878–3885.CrossRefGoogle ScholarPubMed
Costerton, JW, Irvin, RT, Cheng, KJ 1981. The bacterial glycocalyx in nature and disease. Annual Review Microbiology 35, 299–324.CrossRefGoogle ScholarPubMed
Costerton, JW, Cheng, KJ, Geesey, GG, Ladd, TI, Nickel, JC, Dasgupta, M, Marrie, TJ 1987. Bacterial biofilms in nature and disease. Annual Review Microbiology 41, 435–464.CrossRefGoogle ScholarPubMed
Craig, WM, Broderick, GA, Ricker, DB 1987. Quantitation of microorganisms associated with the particulate phase of ruminal ingesta. Journal of Nutrition 117, 56–62.CrossRefGoogle ScholarPubMed
Davis, KE, Joseph, SJ, Janssen, PH 2005. Effects of growth medium, inoculum size, and incubation time on culturability and isolation of soil bacteria. Applied and Environmental Microbiology 71, 826–834.CrossRefGoogle ScholarPubMed
Dehority, BA, Orpin, GC 1997. Development of and natural fluctuations in rumen microbial populations. In The rumen microbial ecosystem (ed. PH Hobson and CS Stewart), pp. 196–245. Chapman & Hall, London, UK.CrossRefGoogle Scholar
Demeyer, DI, Van Nevel, CJ 1979. Effect of defaunation on the metabolism of rumen micro-organisms. British Journal of Nutrition 42, 515–524.CrossRefGoogle Scholar
Dewhurst, RJ, Aston, K, Fisher, WJ, Evans, RT, Dhanoa, MS, McAllan, AB 1999. Comparison of energy and protein sources offered at low levels in grass-silage based diets for dairy cows. Animal Science 68, 789–799.CrossRefGoogle Scholar
Dewhurst, RJ, Davies, DR, Merry, RJ 2000. Microbial protein supply in the rumen. Animal Feed Science and Technology 85, 1–21.CrossRefGoogle Scholar
Eckburg, PB, Bik, EM, Bernstein, CN, Purdom, E, Dethlefsen, L, Sargent, M, Gill, SR, Nelson, KE, Relman, DA 2005. Diversity of the human intestinal microbial flora. Science 308, 1635–1638.CrossRefGoogle ScholarPubMed
Edwards, JE, McEwan, NR, Travis, AJ, Wallace, RJ 2004. 16s rDNA library-based analysis of ruminal bacterial diversity. Antonie van Leeuwenhoek 86, 263–281.CrossRefGoogle Scholar
Edwards, JE, McEwan, NR, McKain, N, Walker, N, Wallace, RJ 2005. Influence of flavomycin on ruminal fermentation and microbial populations in sheep. Microbiology 151, 717–725.CrossRefGoogle ScholarPubMed
Edwards, JE, Huws, SA, Kim, EJ, Kingston-Smith, AH 2007. Characterisation of the dynamics of initial bacterial colonisation of non-conserved forage in the rumen. FEMS Microbiology Ecology 62, 323–335.CrossRefGoogle Scholar
Feller, U 1986. Plant proteolytic enzymes in relation to leaf senescence. In Plant proteolytic enzymes (ed. MJ Dalling), pp. 49–68. CRC Press, Boca Raton, FL, USA.Google Scholar
Gilbert, P, Brown, MRW 1995. Mechanisms of the protection of bacterial biofilms from antimicrobial agents. In Microbial biofilms – plant microbial biotechnology research 5 (ed. HM Lappin-Scott and JW Costerton), Cambridge University Press, Cambridge, UK.Google Scholar
Girvan, MS, Campbell, CD, Killham, K, Prosser, JI, Glover, LA 2005. Bacterial diversity promotes community stability and functional resilience after perturbation. Environmental Microbiology 7, 301–313.CrossRefGoogle ScholarPubMed
Gordon, GLR, Phillips, MW 1998. The role of anaerobic gut fungi in ruminants. Nutrition Research Reviews 11, 133–168.CrossRefGoogle ScholarPubMed
Gregg, K 1995. Engineering gut flora of ruminant livestock to reduce forage toxicity: progress and problems. Trends in Biotechnology 13, 418–421.CrossRefGoogle Scholar
Griffiths, BS, Kuan, HL, Ritz, K, Glover, LA, McCaig, AE, Fenwick, C 2004. The relationship between microbial community structure and functional stability, tested experimentally in an upland pasture soil. Microbial Ecology 47, 104–113.CrossRefGoogle Scholar
Harrison, JJ, Turner, RJ, Marques, LLR, Ceri, H 2005. Biofilms: a new understanding of these microbial communities is driving a revolution that may transform the science of microbiology. American Scientist 93, 508.CrossRefGoogle Scholar
Harstad, OM, Vik-Mo, L 1985. Estimation of microbial and undegraded protein in sheep on grass silage based diets. Acta Agriculturæ Scandinavica 25, 37–48.Google Scholar
Hobson, PN, Stewart, CS 1997. The rumen microbial ecosystem. Chapman & Hall, London, UK.CrossRefGoogle Scholar
Hugenholtz, P 2002. Exploring prokaryotic diversity in the genomic era. Genome Biology 3, 1–8.CrossRefGoogle ScholarPubMed
Hungate, RE 1966. The rumen and its microbes. Academic Press Inc., New York, USA.Google Scholar
Huws, SA, McBain, AJ, Gilbert, P 2005. Protozoan grazing and its impact upon population dynamics in biofilm communities. Journal Applied Microbiology 98, 238–244.CrossRefGoogle ScholarPubMed
Huws, SA, Lee, MRF, Muetzel, S, Wallace, RJ, Scollan, ND 2006. Effect of forage type and level of fish oil inclusion on bacterial diversity in the rumen. Reproduction, Nutrition, Development 46, S99.Google Scholar
Jones, BA, Muck, RE, Hartfield, RD 1995. Red clover extracts inhibit legume proteolysis. Journal of the Science of Food and Agriculture 67, 329–333.CrossRefGoogle Scholar
Kaeberlein, T, Lewis, K, Epstein, SS 2002. Isolating “uncultivable” microorganisms in pure culture in a simulated natural environment. Science 296, 1127–1129.CrossRefGoogle Scholar
Kamra, DN, Pathak, NN 2005. Improvement in livestock productivity by use of probiotics: a review. Indian Journal Animal Science 75, 128–134.Google Scholar
Kim, EJ, Edwards, JE, Sanderson, R, Kingston-Smith, AH, Scollan, ND, Theodorou, MK 2006. Effects of mastication on temporal bacterial colonisation and degradation of fresh perennial ryegrass in the rumen. Reproduction, Nutrition, Development 46, S19.Google Scholar
Kingston-Smith, AH, Theodorou, MK 2000. Post-ingestion metabolism of fresh forage. New Phytologist 148, 37–55.CrossRefGoogle ScholarPubMed
Kingston-Smith, AH, Bollard, AL, Armstead, IP, Thomas, BJ, Theodorou, MK 2003a. Proteolysis and cell death in clover leaves is induced by grazing. Protoplasma 220, 119–129.CrossRefGoogle ScholarPubMed
Kingston-Smith, AH, Bollard, AL, Thomas, BJ, Brooks, AE, Theodorou, MK 2003b. Nutrient availability during the early stages of colonization of fresh forage by rumen micro-organisms. New Phytologist 158, 119–130.CrossRefGoogle Scholar
Kingston-Smith, A, Merry, RJ, Leemans, DK, Thomas, H, Theodorou, MK 2005. Evidence in support of a role of plant-mediated proteolysis in the rumens of grazing animals. British Journal of Nutrition 93, 73–79.CrossRefGoogle ScholarPubMed
Kingston-Smith AH, Davies TE, Edwards JE and Theodorou MK 2008. From plants to animals: the role of plant cell death in ruminant herbivores. Journal of Experimental Botany, doi: 10.1093/jxb/erm326.CrossRefGoogle Scholar
Kobayashi, Y, Forster, RJ, Teather, RM 2000. Development of a competitive polymerase chain reaction assay for the ruminal bacterium Butyrivibrio fibrisolvens OB156-derived recombinant. FEMS Microbiology Letters 188, 185–190.CrossRefGoogle ScholarPubMed
Kobayashi, Y, Koike, S, Taguchi, H, Itabashi, H, Kam, DK, Ha, JK 2004. Recent advances in gut microbiology and their possible contribution to animal health and production – A review. Asian-Australasian Journal of Animal Science 17, 877–884.CrossRefGoogle Scholar
Koike, S, Pan, J, Kobayashi, Y, Tanaka, K 2003. Kinetics of in sacco fiber-attachment of representative ruminal cellulolytic bacteria monitored by competitive PCR. Journal of Dairy Science 86, 1429–1435.CrossRefGoogle ScholarPubMed
Krause, DO, Russell, JB 1996. How many ruminal bacteria are there? Journal of Dairy Science 79, 1467–1475.CrossRefGoogle Scholar
Lafontan, M, Berlan, M, Stich, V, Crampes, F, Riviere, D, De Glisezinski, I, Sengenes, C, Galitzky, J 2002. Recent data on the regulation of lipolysis by catecholamines and natriuretic peptides. Annales D’Endocrinologie 63, 86–90.Google ScholarPubMed
LaRue, R, Yu, Z, Parisi, VA, Egan, AR, Morrison, M 2005. Novel microbial diversity adherent to plant biomass in the herbivore gastrointestinal tract, as revealed by ribosomal intergenic spacer analysis and rrs gene sequencing. Environmental Microbiology 7, 530–543.CrossRefGoogle ScholarPubMed
Lawrence, JR, Snyder, RA 1998. Feeding behaviour and grazing impacts of a Euplotes sp. on attached bacteria. Canadian Journal of Microbiology 44, 623–629.CrossRefGoogle Scholar
Lee, MRF, Harris, LJ, Moorby, JM, Humphreys, MO, Theodorou, MK, MacRae, JC, Scollan, ND 2002. Rumen metabolism and nitrogen flow to the small intestine in steers offered Lolium perenne containing different levels of water-soluble carbohydrate. Animal Science 74, 587–596.CrossRefGoogle Scholar
Lee, MRF, Martinez, EM, Scollan, ND 2003. Plant enzyme mediated lipolysis of Lolium perenne and Trifolium pratense in an in vitro simulated rumen environment. Aspects of Applied Biology 70, 115–120.Google Scholar
Lee, MRF, Winters, AL, Scollan, ND, Dewhurst, RJ, Theodorou, MK, Minchin, FR 2004. Plant mediated lipolysis and proteolysis in red clover with different polyphenol oxidase activities. Journal of the Science of Food and Agriculture 84, 1639–1645.CrossRefGoogle Scholar
Lee, MRF, Tweed, JKS, Moloney, AP, Scollan, ND 2005. The effects of fish oil supplementation on rumen metabolism and the biohydrogenation of unsaturated fatty acids in beef steers given diets containing sunflower oil. Animal Science 80, 361–367.CrossRefGoogle Scholar
Lee, MRF, Parfitt, L, Scollan, ND, Minchin, FR 2007. Lipolysis in red clover with different polyphenol oxidase activities in the presence of rumen fluid. Journal of the Science of Food and Agriculture 87, 1308–1314.CrossRefGoogle Scholar
Mackie, RI, White, BA 1997. Gastrointestinal ecosystems and fermentations. Chapman & Hall, London, UK.CrossRefGoogle Scholar
MacRae, JC, Campbell, DR, Eadie, J 1975. Changes in the biochemical composition of herbage upon freezing and thawing. The Journal of Agricultural Science 84, 125–131.CrossRefGoogle Scholar
Magurran, AE 1988. Ecological diversity and its measurement. Croom Helm, London, UK.CrossRefGoogle Scholar
Marini, JC, Van Amburgh, ME 2005. Partition of nitrogen excretion in urine and the feces of Holstein replacement heifers. Journal of Dairy Science 88, 1778–1784.CrossRefGoogle ScholarPubMed
Mayorga, O, Huws, SA, Kim, EJ, Kingston-Smith, AH, Newbold, CJ, Theodorou, MK 2007. Microbial colonization and subsequent biofilm formation by ruminal microorganisms on fresh perennial ryegrass. Microbial Ecology in Health and Disease 19, 26.Google Scholar
McAllister, TA, Cheng, KJ 1996. Microbial strategies in the ruminal digestion of cereal grains. Animal Feed Science and Technology 62, 29–36.CrossRefGoogle Scholar
McAllister, TA, Rode, LM, Major, DJ, Cheng, KJ, Buchanan-Smith, JG 1990. The effect of ruminal microbial colonization on cereal grain digestion. Canadian Journal of Animal Science 70, 571–579.CrossRefGoogle Scholar
McAllister, TA, Bae, HD, Jones, GA, Cheng, KJ 1994. Microbial attachment and feed digestion in the rumen. Journal of Animal Science 72, 3004–3018.CrossRefGoogle ScholarPubMed
Merry, RJ, Davies, DR, Lee, MRF, Dewhurst, RJ, Moorby, JM, Leemans, DK, Scollan, ND, Theodorou, MK 2006. Effects of high-sugar ryegrass silage and mixtures with red clover silage on ruminant digestion. 1. In vitro and in vivo studies of nitrogen utilization. Journal of Animal Science 84, 3049–3060.CrossRefGoogle ScholarPubMed
Michalet-Doreau, B, Fernandez, I, Peyron, C, Millet, L, Fonty, G 2001. Fibrolytic activities and cellulolytic bacterial community structure in the solid and liquid phases of rumen contents. Reproduction, Nutrition, Development 41, 187–194.CrossRefGoogle ScholarPubMed
Min, BR, Barry, TN, Attwood, GT, McNabb, WC 2003. The effect of condensed tannins on the nutrition and health of ruminants fed fresh temperate forages: a review. Animal Feed Science and Technology 106, 3–19.CrossRefGoogle Scholar
Minato, H, Endo, A, Ootomo, Y, Uemura, T 1966. Ecological treatise on the rumen fermentation. II. The amylolytic and cellulolytic activities of fractionated bacterial portions attached to the rumen solids. The Journal of General and Applied Microbiology 12, 53–69.CrossRefGoogle Scholar
Miron, J, Ben-Ghedalia, D, Morrison, M 2001. Adhesion mechanisms of rumen cellulolytic bacteria. Journal of Dairy Science 84, 1294–1309.CrossRefGoogle ScholarPubMed
Monteny, GJ, Bannink, A, Chadwick, D 2006. Greenhouse gas abatement strategies for animal husbandry. Agriculture, Ecosystems and Environment 112, 163–170.CrossRefGoogle Scholar
Moon-van der Staay, SY, van der Staay, GWM, Javorský, P, Jouany, JP, Michalowski, T, Nsabimana, E, Machebeouf, D, Kišidayová, S, Varadyova, Z, McEwan, NR, Newbold, CJ, Hackstein, JHP 2002. Diversity of rumen ciliates revealed by 18S ribosomal DNA analysis. Reproduction, Nutrition, Development 42, S76.Google Scholar
Nagaraja, TG, Newbold, CJ, Van Nevel, CJ, Demeyer, DI 1997. Manipulation of ruminal fermentation. In The rumen microbial ecosystem (ed. PH Hobson and CS Stewart), pp. 523–632. Chapman & Hall, London, UK.CrossRefGoogle Scholar
Nagaraja, TG, Sun, Y, Wallace, N, Kemp, KE, and Parrott, CJ 1999. Effects of tylosin on concentrations of Fusobacterium necrophorum and fermentation products in the rumen of cattle fed a high-concentrate diet. American Journal of Veterinary Research 60, 1061–1065.CrossRefGoogle ScholarPubMed
Pan, J, Koike, S, Suzuki, T, Ueda, K, Kobayashi, Y, Tanaka, K, Okubo, M 2003. Effect of mastication on degradation of orchardgrass hay stem by rumen microbes: fibrolytic enzyme activities and microbial attachment. Animal Feed Science and Technology 106, 69–79.CrossRefGoogle Scholar
Pederson, K 1990. Biofilm development on stainless steel and PVC surfaces in drinking water. Water Research 24, 239–243.CrossRefGoogle Scholar
Rappe, MS, Giovannoni, SJ 2003. The uncultured microbial majority. Annual Review of Microbiology 57, 369–394.CrossRefGoogle ScholarPubMed
Robinson, PH, Sniffen, CJ, Van Soest, PJ 1985. Influence of level of feed intake on digestion and bacterial yield in the forestomachs of dairy cattle. Canadian Journal of Animal Science 65, 437–444.CrossRefGoogle Scholar
Rooke, JA, Alvarez, P, Armstrong, DG 1986. The digestion by cattle of barley and silage diets containing increasing quantities of soya-bean meal. The Journal of Agricultural Science 107, 263–272.CrossRefGoogle Scholar
Rooke, JA, Lee, NH, Armstrong, DG 1987. The effects of intraruminal infusions of urea, casein, glucose syrup, and a mixture of casein and glucose syrup on nitrogen digestion in the rumen of cattle receiving grass-silage diets. British Journal of Nutrition 32, 89–94.CrossRefGoogle Scholar
Russell, JB, Rychlik, JL 2000. The isolation, characterisation and enumeration of hyper-ammonia producing ruminal bacteria. Asian-Australasian Journal of Animal Sciences 13, 121–127.Google Scholar
Russell, JB, Strobel, HJ 1989. Effect of ionophores on ruminal fermentation. Applied and Environmental Microbiology 55, 1–6.CrossRefGoogle ScholarPubMed
Russell, JB, O’Connor, JD, Fox, DG, Van Soest, PJ, Sniffen, CJ 1992. A net carbohydrate and protein system for evaluating cattle diets: 1. Ruminal fermentation. Journal of Animal Science 70, 3551–3561.CrossRefGoogle ScholarPubMed
Sadet, S, Martin, C, Meunier, B, Morgavi, DP 2007. PCR-DGGE analysis reveals a distinct diversity in the bacterial population attached to the rumen epithelium. Animal 1, 939–944.CrossRefGoogle Scholar
Saginala, S, Nagaraja, TG, Lechtenberg, KF, Chengappa, MM, Kemp, KE, Hine, PM 1997. Effect of Fusobacterium necrophorum leukotoxoid vaccine on susceptibility to experimentally induced liver abscesses in cattle. Journal of Animal Science 75, 1160–1166.CrossRefGoogle ScholarPubMed
Scollan, ND, Hocquette, JF, Nuernberg, K, Dannenberger, D, Richardson, RI, Moloney, AP 2006. Innovations in beef production systems that enhance the nutritional and health value of beef lipids and their relationship with meat quality. Meat Science 74, 17–33.CrossRefGoogle ScholarPubMed
Shi, J, Arunasalam, K, Yeung, D, Kakuda, Y, Mittal, G, Jiang, Y 2004. Saponins from edible legumes: chemistry, processing and health benefits. Journal of Medicinal Food 7, 67–78.CrossRefGoogle ScholarPubMed
Shingfield, KJ, Ahvenjarvi, S, Toivonen, V, Arola, A, Nurmela, KVV, Huhtanen, P, Griinari, JM 2003. Effect of dietary fish oil on biohydrogenation of fatty acids and milk fatty acid content in cows. Animal Science 77, 165–179.CrossRefGoogle Scholar
Siddons, RC, Paradine, J, Gale, DL, Evans, RT 1985. Estimation of the degradability of dietary protein in the sheep rumen by in vivo and in vitro procedures. British Journal of Nutrition 54, 545–561.CrossRefGoogle ScholarPubMed
Sullivan, ML, Hatfield, RD 2006. Polyphenol oxidase and o-diphenols inhibit post harvest proteolysis in red clover and alfalfa. Crop Science 46, 662–670.CrossRefGoogle Scholar
Theodorou, MK, Mennim, G, Davies, DR, Zhu, WY, Trinci, APJ, Brookman, JL 1996. Anaerobic fungi in the digestive tract of mammalian herbivores and their potential for exploitation. Proceedings of the Nutrition Society 55, 913–926.CrossRefGoogle ScholarPubMed
Theodorou MK, Barahona R, Kingston-Smith A, Sanchez S, Lascano C, Owen E and Morris P 2000. New perspectives on the degradation of plant biomass in the rumen in the absence and presence of condensed tannins. In Tannins in livestock and human nutrition (ed. JD Brooker), pp. 44–51. Australian Centre for International Agricultural Research Proceedings Series, 92, Adelaide, Australia.Google Scholar
Thomas, H, Stoddart, JL 1980. Leaf senescence. Annual Review of Plant Physiology 31, 83–111.CrossRefGoogle Scholar
Thomas, PC, Chamberlain, DG, Kelly, NC, Wait, MK 1980. The nutritive value of silages. Digestion of nitrogenous constituents in sheep receiving diets of grass silage and barley. British Journal of Nutrition 43, 469–479.CrossRefGoogle ScholarPubMed
Tilman, D 1996. Biodiversity: population versus ecosystem stability. Ecology 77, 350–363.CrossRefGoogle Scholar
Tuckwell, DS, Nicholson, MJ, McSweeney, CS, Theodorou, MK, Brookman, JL 2005. The rapid assignment of ruminal fungi to presumptive genera using ITS1 and ITS2 RNA secondary structures to produce group-specific fingerprints. Microbiology 151, 1557–1567.CrossRefGoogle ScholarPubMed
Ulyatt, MJ, Beever, DE, Thomson, DJ, Evans, RT, Haines, MJ 1980. Measurement of nutrient supply at pasture. Proceedings of the Nutrition Society 39, 67A.Google Scholar
Vlaeminck, B, Fievez, V, Tamminga, S, Dewhurst, RJ, van Vuuren, AM, De Brabander, D, Demeyer, D 2006. Milk odd- and branched-chain fatty acids in relation to the rumen fermentation pattern. Journal of Dairy Science 89, 3954–3964.CrossRefGoogle Scholar
Wallace, RJ 2004. Antimicrobial properties of plant secondary metabolites. Proceedings of the Nutrition Society 63, 621–629.CrossRefGoogle ScholarPubMed
Wallace, RJ, Onodera, R, Cotta, MA 1997. Metabolism of nitrogen-containing compounds. In The rumen microbial ecosystem (ed. PN Hobson and CS Stewart), pp. 283–328. Chapman & Hall, London, UK.CrossRefGoogle Scholar
Wallace, RJ, Newbold, CJ, Bequette, BJ, MacRae, JC, Lobley, GE 2001. Increasing the flow of protein from ruminal fermentation – review. Asian-Australasian Journal of Animal Science 14, 885–893.CrossRefGoogle Scholar
WHO 2003. Diet, nutrition and prevention of chronic diseases. Report of a joint WHO/FAO expert consultation. WHO Technical Report Series, 916. WHO, Geneva.Google Scholar
Winters, AL, Minchin, FR 2001. Red clover and the future for pasture legumes as an alternative protein source for ruminants. IGER Innovations 5, 30–33.Google Scholar
Wolin, MJ, Miller, TL, Stewart, CS 1997. Microbe–microbe interactions. In The rumen microbial ecosystem (ed. PH Hobson and CS Stewart), pp. 467–491. Chapman & Hall, London, UK.CrossRefGoogle Scholar
Wright, AG, Toovey, AF, Pimm, CL 2006. Molecular identification of methanogenic archaea from sheep in Queensland, Australia reveals more uncultured novel archaea. Anaerobe 12, 134–139.CrossRefGoogle ScholarPubMed
Yu, Z, Yu, M, Morrison, M 2006. Improved serial analysis of V1 ribosomal sequence tags (SARST-V1) provides a rapid, comprehensive, sequence-based characterization of bacterial diversity and community composition. Environmental Microbiology 8, 603–611.CrossRefGoogle ScholarPubMed
Zengler, K, Toledo, G, Rappe, M, Elkins, J, Mathur, EJ, Short, JM, Keller, M 2002. Cultivating the uncultured. Proceedings of the National Academy of Science 99, 15681–15686.CrossRefGoogle ScholarPubMed
Zhu, WY, Kingston-Smith, AH, Troncoso, D, Merry, RJ, Davies, DR, Pichard, G, Thomas, H, Theodorou, MK 1999. Evidence of a role for plant proteases in the degradation of herbage proteins in the rumen of grazing cattle. Journal of Dairy Science 82, 2651–2658.CrossRefGoogle ScholarPubMed