In vitro fermentation patterns and methane production of sainfoin (Onobrychis viciifolia Scop.) hay with different condensed tannin contents

Grass and Forage Science

Volumn 66, Issue 4, 2011, Pages 488-500

  Guglielmelli, A ^a   Calabro S ^a   Primi, R ^b   Carone, F ^a   Cutrignelli, M I ^a   Tudisco, R ^a   Piccolo, G ^a   Ronchi, B ^b   Danieli, P P ^b  

^a UNIVERSITY OF NAPLES FEDERICO II   (Italy)

^b UNIVERSITY OF TUSCIA   (Italy)

Author keywords

Condensed tannins; In vitro gas production; Methane; Onobrychis viciifolia Scop.; Phenological stage

Indexed keywords

ALFALFA; ANAEROBIOSIS; BIODEGRADATION; CHEMICAL COMPOSITION; DIGESTIBILITY; EMISSION INVENTORY; FERMENTATION; FORAGE; LEGUME; METHANE; MICROBIAL ACTIVITY; ORGANIC MATTER; PERENNIAL PLANT; PHENOLOGY; PROTEIN; REACTION KINETICS; RUMINANT; TANNIN;

ANIMALIA; BOVIDAE; DESMODIUM; MEDICAGO SATIVA; ONOBRYCHIS; ONOBRYCHIS VICIIFOLIA;

EID: 80355147092     PISSN: 01425242     EISSN: 13652494     Source Type: Journal    
DOI: 10.1111/j.1365-2494.2011.00805.x     Document Type: Article

References (63)

1. AOAC (2000) Official methods of analysis, 17th edn. Arlington, VA: Association of Official Analytical Chemists.
2. Aufrére J., Dudilieu M. and Poncet C. (2008) In vivo and in situ measurements of the digestive characteristics of sainfoin in comparison with lucerne fed to sheep as fresh forages at two growth stages and as hay. Animal, 2, 1331-1339.
3. Barry T.N., Manley T.R. and Duncan S.J. (1986) The role of condensed tannins in the nutritional value of Lotus pedunculatus for sheep. British Journal of Nutrition, 55, 123-137.
4. Bauer E., Williams B.A., Voigt C., Mosenthin R. and Verstegen M.W.A. (2001) Microbial activities of faeces from unweaned and adult pigs, in relation to selected fermentable carbohydrates. Animal Science, 73, 313-322.
5. Borreani G., Peiretti P.G. and Tabacco E. (2003) Evolution of yield and quality of sainfoin (Onobrychis viciifolia Scop.) in the spring growth cycle. Agronomie, 23, 193-201.
6. Broderick G.A. (1995) Desirable characteristics of forage legumes for improving protein utilization in ruminants. Journal of Animal Science, 73, 2760-2773.
7. Bullard R.W., York J.O. and Kilburn S.R. (1981) Polyphenolic changes in ripening bird-resistant sorghums. Journal of Agricultural and Food Chemistry, 29, 973-981.
8. Butler L.G. (1982) Relative degree of polymerization of sorghum tannin during seed development and maturation. Journal of Agricultural and Food Chemistry, 30, 1090-1094.
9. Calabrò S., Infascelli F., Bovera F., Moniello G. and Piccolo V. (2001) In vitro degradability of three forages: fermentation kinetics and gas production of NDF and neutral detergent soluble fraction of forages. Journal of Science Food and Agriculture, 82, 222-229.
10. Calabrò S., Tudisco R., Balestrieri A., Piccolo G., Infascelli F. and Cutrignelli M.I. (2009) Fermentation characteristics of different grain cultivars with the in vitro gas production technique. Italian Journal of Animal Science, 8, 280-282.
11. Carulla J.E., Kreuzer M., Machmuller A. and Hess H.D. (2005) Supplementation of Acacia mearnsii tannins decreases methanogenesis and urinary nitrogen in forage-fed sheep. Australian Journal of Agricultural Research, 56, 961-970.
12. Doane P.H., Pell A.N. and Schofield P. (1997) The effect of preservation method on the neutral detergent soluble fraction of forages. Journal of Animal Science, 75, 1140-1148.
13. Field J.A., Kortekaas S. and Lettinga G. (1989) The tannin theory of methanogenic toxicity. Journal of Biological Wastes, 29, 241.
14. Frame J., Charlton J.F.L. and Laidlaw A.S. (1998) Alsike clover and sainfoin. In: Frame J., Charlton J.F.L. and Laidlaw A.S. (eds) Temperate forage legumes, pp. 273-289. Wallingford: CAB International.
15. Getachew G., Robinson P.H., DePeters E.J., Taylor S.J., Gisi D.D., Higginbotham G.E. and Riordan T.J. (2005) Methane production from commercial dairy rations estimated using an in vitro gas technique. Animal Feed Science and Technology, 123-124, 391-402.
16. Goering H.K. and Van Soest P.J. (1970) Forage fiber analyses (apparatus, reagents, procedures and some applications). Agricultural Handbook No 379. Washington, DC: US Department of Agriculture.
17. Goldstein J.L. and Swain T. (1963) Changes in tannins in ripening fruits. Phytochemistry, 2, 371-383.
18. Groot J.C.J., Cone J.W., William B.A. and Debersaque F.M.A. (1996) Multiphasic analysis of gas production kinetics for in vitro fermentation of ruminant feedstuff. Animal Feed Science and Technology, 64, 77-89.
19. Hagerman A.E., Robbins C.T., Weerasuriya Y., Wilson T.C. and McArthur C. (1992) Tannin chemistry in relation to digestion. The Journal of Range Management Archives, 45, 57-62.
20. Harrison D.G., Beever D.E., Thomson D.J. and Osbourn D.F. (1973) The influence of diet upon the quantity and types of amino acids entering and leaving the small intestine of sheep. Journal of Agricultural Science, Cambridge, 81, 391-401.
21. Howarth R.E., Goplen B.P., Fesser A.C. and Brandt S.A. (1978) A possible role for leaf cell rupture in legume pasture bloat. Crop Science, 18, 129-133.
22. Jansman A.J.M. (1993) Tannins in feedstuffs for simple-stomached animals. Nutrition and Research Review, 6, 209-236.
23. Johnson K.A. and Johnson D.E. (1995) Methane emissions from cattle. Journal of Animal Science, 73, 2483-2492.
24. Jones W.T., Broadhurst R.B. and Lyttleton J.W. (1976) The condensed tannins of pasture legume species. Phytochemistry, 15, 1407-1409.
25. Jones G.A., McAllister T.A., Muir A.D. and Cheng K.J. (1994) Effect of sainfoin (Onobrichis viciifolia Scop.) condensed tannins on growth and proteolysis by four strains of ruminal bacteria. Applied Environmental Microbiology, 60, 1374-1378.
26. Joseph R., Tanner G. and Larkin P. (1998) Proanthocyanidin synthesis in the forage legume onobrychis viciifolia. a study of chalcone synthase, dihydroflavonol 4-reductase and leucoanthocyanidin 4-reductase in developing leaves. Functional Plant Biology, 25, 271-278.
27. Kallenbach R.L., Matches A.G. and Mahan J.R. (1996) Sainfoin regrowth declines as metabolic rate increases with temperature. Crop Science, 36, 91-97.
28. Kamalak A., Canbolat O., Gurbuz Y., Ozkan C.O. and Kizilsimsek M. (2005) Determination of nutritive value of wild mustard, sinapsis arvensis harvested at different maturity stages using in situ and in vitro measurements. Asian-Australasian Journal of Animal Science, 18, 1249-1254.
29. Kamra D.N. (2005) Rumen microbial ecosystem. Current Science, 89, 124-135.
30. Karnezos T.P., Matches A.G. and Brown C.P. (1994) Spring lamb production on alfalfa, sainfoin, and wheatgrass pastures. Agronomy Journal, 86, 497-502.
31. Koivisto J.M. and Lane G.P.F. (2001) Sainfoin - worth another look. Cirencester, UK: Royal Agricultural College. Available at: (accessed 14 March 2011).
32. Koupai-Abyazani M.R., McCallum J. and Bohm B.A. (1992) Identification of the constituent flavanoid units in sainfoin proanthocyanidins by reversed-phase high-performance liquid chromatography. Journal of Chromatography A, 594, 117-123.
33. Koupai-Abyazani M.R., McCallum J., Muir A.D., Bohm B.A., Towers G.H.N. and Gruber M.Y. (1993) Developmental changes in the composition of proanthocyanidins from leaves of sainfoin (Onobrychis viciifolia Scop.) as determined by HPLC analysis. Journal of Agricultural and Food Chemistry, 41, 1066-1070.
34. Lees G., Suttill N. and Gruber M. (1993) Condensed tannins in sainfoin. 1. A histological and cytological survey of plant tissues. Canadian Journal of Botany, 71, 1147-1152.
35. Lees G., Gruber M. and Suttill N. (1995) Condensed tannins in sainfoin. II. Occurrence and changes during leaf development. Canadian Journal of Botany, 73, 1540-1547.
36. Lovett D.K., McGilloway D., Bortolozzo A., Hawkins M., Callan J., Flynn B. and O'Mara F.P. (2006) In vitro fermentation patterns and methane production as influenced by cultivar and season of harvest of Lolium perenne L. Grass and Forage Science, 61, 9-21.
37. Makkar H.P.S., Blümmel M. and Becker K. (1995) Formation of complexes between polyvinyl pyrrolidones or polyethylene glycols and tannins, and their implication in gas production and true digestibility in vitro techniques. British Journal of Nutrition, 73, 897-913.
38. Marais J.P.J., Mueller-Harvey I., Brandt E.V. and Ferreira D. (2000) Polyphenols, condensed tannins, and other natural products in Onobrychis viciifolia (sainfoin). Journal of Agricultural and Food Chemistry, 48, 3440-3447.
39. Marles S., Bruce M.A., Coulman E. and Bett K.E. (2008) Interference of condensed tannin in lignin analyses of dry bean and forage crops. Journal of Agricultural and Food Chemistry, 56, 9797-9802.
40. Matthews S., Mila I., Scalbert A., Pollet B., Lapierre C. and Herve du Penhoat C.L.M. (1997) Method for estimation of proanthocyanidins based on their acid depolymerization in the presence of nucleophiles. Journal of Agricultural and Food Chemistry, 45, 1195-1201.
41. Mauricio R.M., Owen E.R., Mould F.L., Givens I., Theodorou M.K., France J., Davies D.R. and Dhanoa M.S. (2001) Comparison of bovine rumen fluid and bovine faeces as inoculum for an in vitro gas production technique for evaluating forages. Animal Feed Science and Technology, 89, 33-48.
42. McAllister T.A., Martinez T., Bae H.D., Muir A.D., Yanke L.J. and Jones G.A. (2005) Characterization of condensed tannins purified from legume forages: chromophore production, protein precipitation, and inhibitory effects on cellulose digestion. Journal of Chemical Ecology, 31, 2049-2068.
43. McMahon L.R., Majak W., McAllister T.A., Hall J.W., Jones G.A., Popp J.D. and Cheng K.J. (1999) Effect of sainfoin on in vitro digestion of fresh alfalfa and bloat in steers. Canadian Journal of Animal Science, 79, 203-212.
44. McSweeney C.S., Palmer B., Bunch R. and Krause D.O. (2001) Effect of the tropical forage calliandra on microbial protein synthesis and ecology in the rumen. Journal of Applied Microbiology, 90, 78-88.
45. Min B.R. and Hart S.P. (2002) Tannins for suppression of internal parasites. Journal of Animal Science, 81, 102-109.
46. Min B.R., Barry T.N., Attwood G.T. and McNabb W.C. (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.
47. Moss A.R., Jouany J.P. and Newbold C.J. (2000) Methane production by ruminants: its contribution to global warming. Annales de Zootechnie, 49, 231-253.
48. Palmer B. and McSweeney C.S. (2000) Tannins in Calliandra calothyrsus effect of polyethylene glycol (PEG) and evaluation of 19 accessions. In: Brooker J.D. (ed.), Tannins in livestock and human nutrition. ACIAR Proc. 92, 36-39.
49. Patra A., Kamra D. and Agarwal N. (2005) Effect of plant extracts on in vitro methanogenesis, enzyme activities and fermentation of feed in rumen liquor of buffalo. Animal Feed Science and Technology, 128, 276-291.
50. Price M.L., Van Scoyoc S. and Butler L.G. (1978) A critical evaluation of the vanillin reaction as an assay for tannin in sorghum grain. Journal of Agricultural and Food Chemistry, 26, 1214-1218.
51. Salunke D.K., Chavan J.K. and Kadam S.S. (1990) Dietary tannins: consequences and remedies. Boca Raton, FL: CRC Press.
52. SAS/STAT (2000) User's guide (Release 6.03). Cary, NC: SAS Institute Inc.
53. Schofield P. and Pell A.N. (1995) Measurement and kinetic analysis of the neutral detergent-soluble carbohydrate fraction of legumes and grasses. Journal of Animal Science, 73, 3455-3463.
54. Searle P.L. (1984) Determination of ammonium in seawater based on the indophenol reaction with o-phenylphenol (OPP): a review. Analyst, 109, 549-568.
55. Sileshi Z., Owen E., Dhanoa M.S. and Theodorou M.K. (1996) Prediction of in situ rumen dry matter disappearance of Ethiopian forages from an in vitro gas production technique using a pressure transducer, chemical analyses or in vitro digestibility. Animal Feed Science and Technology, 61, 73-87.
56. Singh S., McCallum J., Gruber M.Y., Neil Towers G.H., Muir A.D. and Bohm B.A. (1997) Biosynthesis of flavan-3-ols by leaf extracts of Onobrychis viciifolia. Phytochemistry, 44, 425-432.
57. Steinfeld H., Gerber P., Vassenaar T., Castel V., Rosales M. and De Haan C. (eds) (2006) Livestock's long shadow. Environmental issues and options. Rome: FAO. Available at: (accessed 14 March 2011).
58. Theodorou M.K., Williams B.A., Dhanoa M.S., McAllan A.B. and France J. (1994) A simple gas production method using a pressure transducer to determine the fermentation kinetics of ruminant feeds. Animal Feed Science and Technology, 48, 185-197.
59. Van Soest P.J. (1994) Nutritional ecology of the ruminant, 2nd edn. Ithaca, New York: Cornell University Press.
60. Waghorn G. (1996) Condensed tannins and nutrient absorption from the small intestine. In: Rode L.M. (ed.), Proceedings of the 1996 Canadian Society of Animal Science Meeting Lethbridge Ab. July 7-11, pp. 175-194.
61. Waghorn G. (2008) Beneficial and detrimental effects of dietary condensed tannins for sustainable sheep and goat production - progress and challenges. Animal Feed Science and Technology, 147, 116-139.
62. Wang Y., Barbieri L., Berg B. and McAllister T. (2007) Effects of mixing sainfoin with alfalfa on ensiling, ruminal fermentation and total tract digestion of silage. Animal Feed Science and Technology, 1353, 296-314.
63. Zielinski H. and Kozlowska H. (2000) Antioxidant activity and total phenolics in selected cereal grains and their different morphological fractions. Journal of Agricultural and Food Chemistry, 48, 2008-2016.