Hostname: page-component-8448b6f56d-t5pn6 Total loading time: 0 Render date: 2024-04-20T03:50:33.582Z Has data issue: false hasContentIssue false

Developing a conceptual model of possible benefits of condensed tannins for ruminant production

Published online by Cambridge University Press:  01 May 2014

L. O. Tedeschi*
Affiliation:
Department of Animal Science, Texas A&M University, College Station, TX 77843-2471, USA CSIRO Animal Food and Health Sciences, James Cook University, Townsville, QLD 4814, Australia
C. A. Ramírez-Restrepo
Affiliation:
CSIRO Animal Food and Health Sciences, James Cook University, Townsville, QLD 4814, Australia
J. P. Muir
Affiliation:
Texas A&M AgriLife Research, Texas A&M University, 1229 North U.S. Hwy 281, Stephenville, TX 76401, USA
Get access

Abstract

Enteric methane (CH4) emissions from ruminants have compelled a wide range of research initiatives to identify environmental abatement opportunities. However, although such mitigations can theoretically be attained with feed additives and feeding strategies, the limited empirical evidence on plant extracts used as feed additives does not support extensive or long-term reductions. Nevertheless, their strategic use (i.e. alone or combined in a simultaneous or consecutive use) may provide not only acceptable CH4 abatement levels, but also relevant effects on animal physiology and productivity. Condensed tannins (CT) represent a range of polyphenolic compounds of flavan-3-ol units present in some forage species that can also be added to prepared diets. Methods to determine CT, or their conjugated metabolites, are not simple. Although there are limitations and uncertainties about the methods to be applied, CT are thought to reduce CH4 production (1) indirectly by binding to the dietary fibre and/or reducing the rumen digestion and digestibility of the fibre and (2) directly by inhibiting the growth of rumen methanogens. On the basis of their role in livestock nutrition, CT influence the digestion of protein in the rumen because of their affinity for proteins (e.g. oxidative coupling and H bonding at neutral pH) that causes the CT-protein complex to be insoluble in the rumen; and dissociate in the abomasum at pH 2.5 to 3.0 for proteolysis and absorption in the small intestine. CT may also reduce gastro-intestinal parasite burdens and improve reproductive performance, foetal development, immune system response, hormone serum concentrations, wool production and lactation. The objectives of this paper are to discuss some of the beneficial and detrimental effects of CT on ruminant production systems and to develop a conceptual model to illustrate these metabolic relationships in terms of systemic physiology using earlier investigations with the CT-containing legume Lotus corniculatus. Our conceptual model indicated four complex and long-lasting relationships (digestive, toxicological, physiological and morphological) that can alter the normal biology of the animal. These relationships are interdependent, integrative, and sometimes, complementary to each other. This conceptual model can be used to develop mechanistic models to improve the understanding of the interaction between CT and the ruminants as well as to guide research initiatives of the impact of polyphenol-rich foods on human health.

Type
Full Paper
Copyright
© The Animal Consortium 2014 

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

Aerts, RJ, Barry, TN and McNabb, WC 1999. Polyphenols and agriculture: beneficial effects of proanthocyanidins in forages. Agriculture, Ecosystems & Environment 75, 112.CrossRefGoogle Scholar
Ammar, H, López, S, González, JS and Ranilla, MJ 2004. Comparison between analytical methods and biological assays for the assessment of tannin-related antinutritive effects in some Spanish browse species. Journal of the Science of Food and Agriculture 84, 13491356.CrossRefGoogle Scholar
Barry, TN and Duncan, SJ 1984. The role of condensed tannins in the nutritional value of Lotus pedunculatus for sheep. 1. Voluntary intake. British Journal of Nutrition 51, 485491.CrossRefGoogle ScholarPubMed
Barry, TN and Manley, TR 1984. The role of condensed tannins in the nutritional value of Lotus pedunculatus for sheep. 2. Quantitative digestion of carbohydrates and proteins. British Journal of Nutrition 51, 493504.CrossRefGoogle ScholarPubMed
Barry, TN and Blaney, BJ 1987. Secondary compounds of forages. In The nutrition of herbivores (ed. JB Hacker and JH Ternouth), pp. 91120. Academic Press, New York, NY.Google Scholar
Barry, TN and McNabb, WC 1999. The implications of condensed tannins on the nutritive value of temperate forages fed to ruminants. British Journal of Nutrition 81, 263272.CrossRefGoogle ScholarPubMed
Barry, TN, Allsop, TF and Redekopp, C 1986a. The role of condensed tannins in the nutritional value of Lotus pedunculatus for sheep. 5. Effects on the endocrine system and on adipose tissue metabolism. British Journal of Nutrition 56, 607614.CrossRefGoogle ScholarPubMed
Barry, TN, Manley, TR and Duncan, SJ 1986b. The role of condensed tannins in the nutritional value of Lotus pedunculatus for sheep. 4. Sites of carbohydrate and protein digestion as influenced by dietary reactive tannin concentration. British Journal of Nutrition 55, 123137.CrossRefGoogle ScholarPubMed
Barry, TN, Kemp, PD, Ramirez-Restrepo, CA and Lopez-Villalobos, N 2003. Sheep production and agronomic performance of Lotus corniculatus under dryland farming. Proceedings of the New Zealand Grassland Association, Palmerston North, NZ, pp. 109−116.Google Scholar
Barry, TN, Parkinsin, TJ, Ramirez-Restrepo, CA, McWilliam, EL and Lopez-Villalobos, N 2004. Can mating ewes on condensed tannin-containing forages be used to reduce lamb mortality between birth and weaning? Proceedings of the New Zealand Society of Animal Production, Hamilton, New Zealand, pp. 30−33.Google Scholar
Barry, TN, McNabb, WC, Kemp, PD, Waghorn, GC, Min, BR and Luque, A 1999. The effect of condensed tannins in Lotus corniculatus upon reproductive efficiency and wool production in sheep during late summer and autumn. Proceedings of the New Zealand Grassland Association, West Coast, pp. 51−55.CrossRefGoogle Scholar
Beauchemin, KA, McGinn, SM, Martinez, TF and McAllister, TA 2007. Use of condensed tannin extract from quebracho trees to reduce methane emissions from cattle. Journal of Animal Science 85, 19901996.CrossRefGoogle ScholarPubMed
Benoit, RE and Starkey, RL 1968. Inhibition of decomposition of cellulose and some other carbohydrates by tannin. Soil Science 105, 291296.CrossRefGoogle Scholar
Beuselinck, PR and Grant, WF 1995. Birdsfoot trefoil. In Forages; an introduction to grassland agriculture (ed. RF Barnes, DA Miller and CJ Nelson), pp. 237248. Iowa State University Press, Ames, IA.Google Scholar
Carter, EB, Theodorou, MK and Morris, P 1999. Responses of Lotus corniculatus to environmental change. 2. Effect of elevated CO2, temperature and drought on tissue digestion in relation to condensed tannin and carbohydrate accumulation. Journal of the Science of Food and Agriculture 79, 14311440.3.0.CO;2-4>CrossRefGoogle Scholar
Chanet, A, Milenkovic, D, Claude, S, Maier, JAM, Kamran Khan, M, Rakotomanomana, N, Shinkaruk, S, Bérard, AM, Bennetau-Pelissero, C, Mazur, A and Morand, C 2013. Flavanone metabolites decrease monocyte adhesion to TNF-α-activated endothelial cells by modulating expression of atherosclerosis-related genes. British Journal of Nutrition 110, 587598.CrossRefGoogle ScholarPubMed
Cieslak, A, Szumacher-Strabel, M, Stochmal, A and Oleszek, W 2013. Plant components with specific activities against rumen methanogens. Animal 7, 253265.CrossRefGoogle ScholarPubMed
Davis, SL, Garrigus, US and Hinds, FC 1970a. Metabolic effects of growth hormone and diethylstilbestrol in lambs. II. Effects of daily ovine growth hormone injections on plasma metabolites and nitrogen-retention in fed lambs. Journal of Animal Science 30, 236240.CrossRefGoogle ScholarPubMed
Davis, SL, Garrigus, US and Hinds, FC 1970b. Metabolic effects of growth hormone and diethylstilbestrol in lambs. III. Metabolic effects of Des. Journal of Animal Science 30, 241244.CrossRefGoogle Scholar
del Pino, MCÁ, Hervás, G, Mantecón, ÁR, Giráldez, FJ and Frutos, P 2005. Comparison of biological and chemical methods, and internal and external standards, for assaying tannins in Spanish shrub species. Journal of the Science of Food and Agriculture 85, 583590.CrossRefGoogle Scholar
Douglas, GB, Wang, Y, Waghorn, GC, Barry, TN, Purchas, RW, Foote, AG and Wilson, GF 1995. Liveweight gain and wool production of sheep grazing Lotus corniculatus and lucerne (Medicago sativa). New Zealand Journal of Agricultural Research 38, 95104.CrossRefGoogle Scholar
Feeny, P 1976. Plant apparency and chemical defense. Recent Advances in Phytochemistry 10, 140.Google Scholar
Fletcher, LR, Sutherland, BL and Fletcher, CG 1999. The impact of endophyte on the health and productivity of sheep grazing ryegrass-based pastures. Ryegrass Endophyte: An Essential New Zealand Symbiosis (Grassland Research and Practice Series, 7), New Zealand Grassland Association, Napier, NZ, pp. 11−17.CrossRefGoogle Scholar
Foo, LY, Lu, Y, McNabb, WC, Waghorn, G and Ulyatt, MJ 1997. Proanthocyanidins from Lotus pedunculatus . Phytochemistry 45, 16891696.CrossRefGoogle Scholar
Foo, LY, Newman, R, Waghorn, G, McNabb, WC and Ulyatt, MJ 1996. Proanthocyanidins from Lotus corniculatus . Phytochemistry 41, 617624.CrossRefGoogle Scholar
Forkner, RE, Marquis, RJ and Lill, JT 2004. Feeny revisited: condensed tannins as anti-herbivore defences in leaf-chewing herbivore communities of Quercus. Ecological Entomology 29, 174187.CrossRefGoogle Scholar
Gebrehiwot, L, Beuselinck, PR and Roberts, CA 2002. Seasonal variations in condensed tannin concentration of three Lotus species. Agronomy Journal 94, 10591065.CrossRefGoogle Scholar
Georgi, JR 1985. Parasitology for veterinarians. Saunders, New York, NY.Google Scholar
Giner-Chavez, BI, Van Soest, PJ, Robertson, JB, Lascano, C, Reed, JD and Pell, AN 1997. A method for isolating condensed tannins from crude plant extracts with trivalent Ytterbium. Journal of the Science of Food and Agriculture 74, 359368.3.0.CO;2-C>CrossRefGoogle Scholar
Hagerman, AE and Butler, LG 1978. Protein precipitation method for the quantitative determination of tannins. Journal of Agricultural and Food Chemistry 26, 809812.CrossRefGoogle Scholar
Hedqvist, H, Mueller-Harvey, I, Reed, JD, Krueger, CG and Murphy, M 2000. Characterisation of tannins and in vitro protein digestibility of several Lotus corniculatus varieties. Animal Feed Science and Technology 87, 4156.CrossRefGoogle Scholar
Hegarty, RS, Goopy, JP, Herd, RM and McCorkell, B 2007. Cattle selected for lower residual feed intake have reduced daily methane production. Journal of Animal Science 85, 14791486.CrossRefGoogle ScholarPubMed
Heil, M, Baumann, B, Andary, C, Linsenmair, E and McKey, D 2002. Extraction and quantification of ‘condensed tannins’ as a measure of plant anti-herbivore defence? Revisiting an old problem. Naturwissenschaften 89, 519524.CrossRefGoogle ScholarPubMed
Holderness, J, Jackiw, L, Kimmel, E, Kerns, H, Radke, M, Hedges, JF, Petrie, C, McCurley, P, Glee, PM, Palecanda, A and Jutila, MA 2007. Select plant tannins induce IL-2Rα up-regulation and augment cell division in γδ T cells. The Journal of Immunology 179, 64686478.CrossRefGoogle ScholarPubMed
Hoste, H, Jackson, F, Athanasiadou, S, Thamsborg, SM and Hoskin, SO 2006. The effects of tannin-rich plants on parasitic nematodes in ruminants. Trends in Parasitology 22, 253261.CrossRefGoogle ScholarPubMed
Jones, DA and Turkington, R 1986. Biological flora of the British Isles. Lotus Corniculatus L. Journal of Ecology 74, 11851212.CrossRefGoogle Scholar
Jones, WT and Mangan, JL 1977. Complexes of the condensed tannins of sainfoin (Onobrychis viciifolia scop.) with fraction 1 leaf protein and with submaxillary mucoprotein, and their reversal by polyethylene glycol and pH. Journal of the Science of Food and Agriculture 28, 126136.CrossRefGoogle Scholar
Jones, WT, Anderson, LB and Ross, MD 1973. Bloat in cattle. New Zealand Journal of Agricultural Research 16, 441446.CrossRefGoogle Scholar
Jutila, MA, Holderness, J, Graff, JC and Hedges, JF 2008. Antigen-independent priming: a transitional response of bovine γδ T-cells to infection. Animal Health Research Reviews 9, 4757.CrossRefGoogle ScholarPubMed
Kabelitz, D and Wesch, D 2003. Features and functions of γδ T lymphocytes: Focus on chemokines and their receptors. Critical Reviews in Immunology 23, 32.CrossRefGoogle Scholar
Leathwick, DM and Atkinson, DS 1995. Dagginess and flystrike in lambs grazed on Lotus corniculatus or ryegrass. Proceedings of the New Zealand Society of Animal Production, Hamilton, New Zealand, pp. 196−198.Google Scholar
Leathwick, DM and Atkinson, DS 1998. Influence of different proportions of Lotus corniculatus in the diet of lambs on dags, flystrike and animal performance. Wool Technology and Sheep Breeding 46, 353359.Google Scholar
Li, Y-G, Tanner, G and Larkin, P 1996. The DMACA–HCl protocol and the threshold proanthocyanidin content for bloat safety in forage legumes. Journal of the Science of Food and Agriculture 70, 89101.3.0.CO;2-N>CrossRefGoogle Scholar
MacAdam, JW, Ward, RE, Griggs, TC, Min, BR and Aiken, GE 2011. Case study: average daily gain and blood fatty acid composition of cattle grazing the nonbloating legumes birdsfoot trefoil and Cicer milkvetch in the Mountain West. The Professional Animal Scientist 27, 574583.CrossRefGoogle Scholar
Majewski, AC, Tekin, S and Hansen, PJ 2001. Local versus systemic control of numbers of endometrial T cells during pregnancy in sheep. Immunology 102, 317322.CrossRefGoogle ScholarPubMed
Makkar, HPS, Gamble, G and Becker, K 1999. Limitation of the butanol–hydrochloric acid–iron assay for bound condensed tannins. Food Chemistry 66, 129133.CrossRefGoogle Scholar
Mangan, JL 1988. Nutritional effects of tannins in animal feeds. Nutrition Research Reviews 1, 209231.CrossRefGoogle ScholarPubMed
Martin, J and Martin, M 1982. Tannin assays in ecological studies: lack of correlation between phenolics, proanthocyanidins and protein-precipitating constituents in mature foliage of six oak species. Oecologia 54, 205211.CrossRefGoogle ScholarPubMed
McLeod, MN 1974. Plant tannins-their role in forage quality. Nutrition Abstracts and Reviews 44, 803815.Google Scholar
Ministry of Agriculture, Fisheries and Food. 1986. Manual of veterinary parasitological laboratory techniques. Her Majesty’s Stationery Office, London, UK.Google Scholar
Molan, AL, Waghorn, GC and McNabb, WC 1999. Condensed tannins and gastro-intestinal parasites in sheep. Proceedings of the New Zealand Grassland Association, West Coast, pp. 57−61.CrossRefGoogle Scholar
Molan, AL, McNabb, WC, Hoskin, SO and Barry, TN 2000. Effect of condensed tannins extracted from four forages on the viability of the larvae of deer lungworms and gastrointestinal nematodes. Veterinary Record 147, 4448.CrossRefGoogle ScholarPubMed
Molan, AL, Duncan, AJ, Barry, TN and McNabb, WC 2003. Effects of condensed tannins and crude sesquiterpene lactones extracted from chicory on the motility of larvae of deer lungworm and gastrointestinal nematodes. Parasitology International 52, 209218.CrossRefGoogle ScholarPubMed
Mueller-Harvey, I 2006. Unravelling the conundrum of tannins in animal nutrition and health. Journal of the Science of Food and Agriculture 86, 20102037.CrossRefGoogle Scholar
Mueller-Harvey, I and Mcallan, AB 1992. Tannins: their biochemistry and nutritional properties. In Advances in plant cell biochemistry and biotechnology (ed. IM Morrison), pp. 151217. JAI Press, London.Google Scholar
Muir, JP 2011. The multi-faceted role of condensed tannins in the goat ecosystem. Small Ruminant Research 98, 115120.CrossRefGoogle Scholar
Muir, LA, Wien, S, Duquette, PF, Rickes, EL and Cordes, EH 1983. Effects of exogenous growth hormone and diethylstilbestrol on growth and carcass composition of growing lambs. Journal of Animal Science 56, 13151323.CrossRefGoogle ScholarPubMed
Mupeyo, B, Barry, TN, Pomroy, WE, Ramírez-Restrepo, CA, López-Villalobos, N and Pernthaner, A 2011. Effects of feeding willow (Salix spp.) upon death of established parasites and parasite fecundity. Animal Feed Science and Technology 164, 820.CrossRefGoogle Scholar
Naumann, HD, Muir, JP, Lambert, BD, Tedeschi, LO and Kothmann, M 2013a. Condensed tannins in the ruminant environment: a perspective on biological activity. Journal of Agricultural Sciences 1, 820.Google Scholar
Naumann, HD, Tedeschi, LO, Muir, JP, Lambert, BD and Kothmann, MM 2013b. Effect of molecular weight of condensed tannins from warm-season perennial legumes on ruminal methane production in vitro . Biochemical Systematics and Ecology 50, 154162.CrossRefGoogle Scholar
Niezen, JH, Waghorn, TS, Charleston, WAG and Waghorn, GC 1995. Growth and gastrointestinal nematode parasitism in lambs grazing either lucerne (Medicago sativa) or sulla (Hedysarum coronarium) which contains condensed tannins. The Journal of Agricultural Science 125, 281289.CrossRefGoogle Scholar
Niezen, JH, Robertson, HA, Waghorn, GC, Charleston, WAG 1998. Production, faecal egg counts and worm burdens of ewe lambs which grazed six contrasting forages. Veterinary Parasitology 80, 1527.CrossRefGoogle ScholarPubMed
Novobilský, A, Mueller-Harvey, I and Thamsborg, SM 2011. Condensed tannins act against cattle nematodes. Veterinary Parasitology 182, 213220.CrossRefGoogle ScholarPubMed
Oliveira, LJ, Barreto, RSN, Perecin, F, Mansouri-Attia, N, Pereira, FTV and Meirelles, FV 2012. Modulation of maternal immune system during pregnancy in the cow. Reproduction in Domestic Animals 47, 384393.CrossRefGoogle ScholarPubMed
Ott, TL, Yin, J, Wiley, AA, Kim, H-T, Gerami-Naini, B, Spencer, TE, Bartol, FF, Burghardt, RC and Bazer, FW 1998. Effects of the estrous cycle and early pregnancy on uterine expression of Mx protein in sheep (Ovis aries). Biology of Reproduction 59, 784794.CrossRefGoogle ScholarPubMed
Percival, SS, Bukowski, JF and Milner, J 2008. Bioactive food components that enhance γδ T cell function may play a role in cancer prevention. The Journal of Nutrition 138, 14.CrossRefGoogle ScholarPubMed
Ramírez-Restrepo, CA 2004. Nutritional studies on Lotus corniculatus containing condensed tannins to increase reproductive rate and lamb growth under commercial dryland farming conditions. Thesis PhD, Massey University, Palmerston North, New Zealand.Google Scholar
Ramírez-Restrepo, CA and Barry, TN 2005. Alternative temperate forages containing secondary compounds for improving sustainable productivity in grazing ruminants. Animal Feed Science and Technology 120, 179201.CrossRefGoogle Scholar
Ramírez-Restrepo, CA, Barry, TN and López-Villalobos, N 2006a. Organic matter digestibility of condensed tannin-containing Lotus corniculatus and its prediction in vitro using cellulase/hemicellulase enzymes. Animal Feed Science and Technology 125, 6171.CrossRefGoogle Scholar
Ramírez-Restrepo, CA, Kemp, PD, Barry, TN and López‐Villalobos, N 2006b. Production of Lotus corniculatus L. under grazing in a dryland farming environment. New Zealand Journal of Agricultural Research 49, 89100.CrossRefGoogle Scholar
Ramírez-Restrepo, CA, Barry, TN, López-Villalobos, N, Kemp, PD and McNabb, WC 2004. Use of Lotus corniculatus containing condensed tannins to increase lamb and wool production under commercial dryland farming conditions without the use of anthelmintics. Animal Feed Science and Technology 117, 85105.CrossRefGoogle Scholar
Ramírez-Restrepo, CA, Barry, TN, López-Villalobos, N, Kemp, PD and Harvey, TG 2005a. Use of Lotus corniculatus containing condensed tannins to increase reproductive efficiency in ewes under commercial dryland farming conditions. Animal Feed Science and Technology 121, 2343.CrossRefGoogle Scholar
Ramírez-Restrepo, CA, Barry, TN, Pomroy, WE, López-Villalobos, N, McNabb, WC and Kemp, PD 2005b. Use of Lotus corniculatus containing condensed tannins to increase summer lamb growth under commercial dryland farming conditions with minimal anthelmintic drench input. Animal Feed Science and Technology 122, 197217.CrossRefGoogle Scholar
Ramírez-Restrepo, CA, Barry, TN, Marriner, A, López-Villalobos, N, McWilliam, EL, Lassey, KR and Clark, H 2010a. Effects of grazing willow fodder blocks upon methane production and blood composition in young sheep. Animal Feed Science and Technology 155, 3343.CrossRefGoogle Scholar
Ramírez-Restrepo, CA, Pernthaner, A, Barry, TN, López-Villalobos, N, Shaw, RJ, Pomroy, WE and Hein, WR 2010b. Characterization of immune responses against gastrointestinal nematodes in weaned lambs grazing willow fodder blocks. Animal Feed Science and Technology 155, 99110.CrossRefGoogle Scholar
Reid, CSW, Ulyatt, MJ and Wilson, JM 1974. Plant tannins, bloat and nutritive value. Proceedings of the New Zealand Society of Animal Production, Hamilton, New Zealand, pp. 82−93.Google Scholar
Sivakumaran, S, Rumball, W, Lane, G, Fraser, K, Foo, L, Yu, M and Meagher, L 2006. Variation of proanthocyanidins in Lotus species. Journal of Chemical Ecology 32, 17971816.CrossRefGoogle ScholarPubMed
Sterman, JD 2000. Business dynamics: systems thinking and modeling for a complex world. Irwin McGraw-Hill, New York, NY.Google Scholar
Sterman, JD 2001. System dynamics modeling: tools for learning in a complex world. California Management Review 43, 825.CrossRefGoogle Scholar
Stewart, HJ 1992. Ovine and bovine type I trophoblast interferon synthesized by the early embryo during the period of the maternal recognition of pregnancy. Protein Engineering: Proceedings of an AFRC Conference on Protein Engineering in the Agricultural and Food Industry, Selwyn College, Cambridge, pp. 81−94.Google Scholar
Swain, T 1979. Tannins and lignins. In Herbivores, their interactions with secondary plant metabolites (ed. GA Rosenthal, DH Janzen and SW Applebaum), pp. 657682. Academic Press, New York, NY.Google Scholar
Tanner, G, Moate, P, Davis, L, Laby, R, Li, Y, Larkin, P and Li, Y 1995. Proanthocyanidins (condensed tannin) destabilise plant protein foams in a dose dependent manner. Australian Journal of Agricultural Research 46, 11011109.CrossRefGoogle Scholar
Tavendale, MH, Meagher, LP, Pacheco, D, Walker, N, Attwood, GT and Sivakumaran, S 2005. Methane production from in vitro rumen incubations with Lotus pendunculatus and Medicago sativa, and effects of extractable condensed tannin fractions on methanogenesis. Animal Feed Science and Technology 123−124, 403419.CrossRefGoogle Scholar
Tedeschi, LO, Fox, DG and Tylutki, TP 2003. Potential environmental benefits of ionophores in ruminant diets. Journal of Environmental Quality 32, 15911602.CrossRefGoogle ScholarPubMed
Tedeschi, LO, Nicholson, CF and Rich, E 2011a. Using system dynamics modelling approach to develop management tools for animal production with emphasis on small ruminants. Small Ruminant Research 98, 102110.CrossRefGoogle Scholar
Tedeschi, LO, Callaway, TR, Muir, JP and Anderson, R 2011b. Potential environmental benefits of feed additives and other strategies for ruminant production. Revista Brasileira de Zootecnia 40, 291309.Google Scholar
Tekin, Ş and Hansen, PJ 2004. Regulation of numbers of macrophages in the endometrium of the sheep by systemic effects of pregnancy, local presence of the conceptus, and progesterone. American Journal of Reproductive Immunology 51, 5662.CrossRefGoogle Scholar
Terrill, TH, Rowan, AM, Douglas, GB and Barry, TN 1992. Determination of extractable and bound condensed tannin concentrations in forage plants, protein concentrate meals and cereal grains. Journal of the Science of Food and Agriculture 58, 321329.CrossRefGoogle Scholar
Terrill, TH, Waghorn, GC, Woolley, DJ, McNabb, WC and Barry, TN 1994. Assay and digestion of 14C-labelled condensed tannins in the gastrointestinal tract of sheep. British Journal of Nutrition 72, 467477.CrossRefGoogle ScholarPubMed
Turkington, ROY and Franko, GD 1980. The biology of Canadian weeds. 41. Lotus corniculatus L. Canadian Journal of Plant Science 60, 965979.CrossRefGoogle Scholar
Van Soest, PJ 1994. Nutritional ecology of the ruminant. Comstock Publishing Associates, Ithaca, NY.CrossRefGoogle Scholar
Waghorn, GC and Hegarty, RS 2011. Lowering ruminant methane emissions through improved feed conversion efficiency. Animal Feed Science and Technology 166−167, 291301.CrossRefGoogle Scholar
Waghorn, GC, Tavendale, MH and Woodfield, DR 2002. Methanogenesis from forages fed to sheep. Proceedings of the New Zealand Grassland Association, West Coast, pp. 167−171.CrossRefGoogle Scholar
Waghorn, GC, Ulyatt, MJ, John, A and Fisher, MT 1987. The effect of condensed tannins on the site of digestion of amino acids and other nutrients in sheep fed on Lotus corniculatus L. British Journal of Nutrition 57, 115126.CrossRefGoogle ScholarPubMed
Waghorn, GC, Shelton, ID, McNabb, WC and McCutcheon, SN 1994. Effects of condensed tannins in Lotus pedunculatus on its nutritive value for sheep. 2. Nitrogenous aspects. The Journal of Agricultural Science 123, 109119.CrossRefGoogle Scholar
Walker, CG and Mitchell, MD 2013. Reproductive technologies for the future: a role for epigenetics. Animal Production Science 53, 954964.CrossRefGoogle Scholar
Wang, Y, Douglas, GB, Waghorn, GC, Barry, TN and Foote, AG 1996. Effect of condensed tannins in Lotus corniculatus upon lactation performance in ewes. The Journal of Agricultural Science 126, 353362.CrossRefGoogle Scholar
Wen, L, Kallenbach, RL, Williams, JE, Roberts, CA, Beuselinck, PR, McGraw, RL and Benedict, HR 2002. Performance of steers grazing rhizomatous and nonrhizomatous birdsfoot trefoil in pure stands and in tall fescue mixtures. Journal of Animal Science 80, 19701976.CrossRefGoogle ScholarPubMed
Wharton, D 1980. Nematode egg-shells. Parasitology 81, 447463.CrossRefGoogle ScholarPubMed
Woodward, SL, Waghorn, GC and Laboyre, P 2004. Condensed tannins in birdsfoot trefoil (Lotus corniculatus) reduced methane emissions from dairy cows. Proceedings of the New Zealand Society of Animal Production, Hamilton, New Zealand, pp. 160−164.Google Scholar
Woodward, SL, Chaves, AV, Waghorn, GC, Brookes, IM and Burke, JL 2006. Supplementing fresh pasture with maize, lotus, sulla and pasture silages for dairy cows in summer. Journal of the Science of Food and Agriculture 86, 12631270.CrossRefGoogle Scholar
Xie, D-Y and Dixon, RA 2005. Proanthocyanidin biosynthesis – still more questions than answers? Phytochemistry 66, 21272144.CrossRefGoogle ScholarPubMed