Hostname: page-component-cd9895bd7-lnqnp Total loading time: 0 Render date: 2024-12-23T10:40:13.897Z Has data issue: false hasContentIssue false

Sainfoin (Onobrychis viciifolia): a beneficial forage legume

Published online by Cambridge University Press:  04 March 2011

Christine Hayot Carbonero
Affiliation:
National Institute of Agricultural Botany, Cambridge CB3 0LE, UK
Irene Mueller-Harvey
Affiliation:
Department of Agriculture, University of Reading, Reading RG6 6AT, UK
Terence A. Brown
Affiliation:
Manchester Interdisciplinary Biocentre, Faculty of Life Sciences, University of Manchester, Manchester M1 7DN, UK
Lydia Smith*
Affiliation:
National Institute of Agricultural Botany, Cambridge CB3 0LE, UK
*
*Corresponding author. E-mail: [email protected]

Abstract

The Onobrychis genus comprises a few agronomically important forage legume species, with sainfoin (Onobrychis viciifolia) being the most widespread. O. viciifolia has a long history of traditional culture worldwide, but its use has declined in western countries over the last decades. It suffers from low productivity and is more difficult to maintain than other legumes but is known to have valuable characteristics such as palatability and drought tolerance. Recent studies suggest that it has several other highly beneficial properties due to its unique tannin and polyphenol composition. Condensed tannins present in Onobrychis species have been shown to confer anthelmintic properties, increase protein utilization and prevent bloating; they may also have the potential to reduce greenhouse gas emissions. Positive effects on wildlife and honey production could also be advantageous in the context of sustainable farming. Modern breeding programmes have not been a priority, leading to a lack of genetic knowledge in comparison to extensively used forage legumes. It is expected that potential for O. viciifolia improvements could be achieved by rigorous characterization of the available germplasm and utilization of characters derived from close relatives of the genus. Breeding priorities for the future would include enhanced germination and improved early establishment, allied to the best anthelmintic properties observed in some varieties.

Type
Research Article
Copyright
Copyright © NIAB 2011

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

Abou-El-Enain, MM (2002) Chromosomal criteria and their phylogenetic implications in the genus Onobrychis Mill. sect. Lophobrychis (Leguminosae), with special reference to Egyptian species. Botanical Journal of the Linnean Society 139: 409414.CrossRefGoogle Scholar
Ahangarian, S, Kazempour Osaloo, Sh and Maassoumi, AA (2007) Molecular phylogeny of the tribe Hedysareae with special reference to Onobrychis (Fabaceae) as inferred from nrDNA ITS sequences. Iran Journal of Botany 13: 6474.Google Scholar
Ahmad, AF, Thill, J, Regos, I, Hayot, C, Halbwirth, H, Smith, LMJ, Treutter, D and Stich, K (2010) Biosynthesis of flavonoids in sainfoin (Onobrychis viciifolia). Poster presented at the 25th International Conference on Polyphenols, 23–27 August 2010, Montpellier, France.Google Scholar
Albrecht, KA and Muck, RE (1991) Proteolysis in ensiled forage legumes that vary in tannin concentration. Crop Science 31: 464469.CrossRefGoogle Scholar
Aston, D, Carreck, N, Davis, I, Lovett, T and Metcalf, P (2009) British Beekeepers’ Association. Honey bee health – research concepts. http://www.britishbee.org.uk/files/bbka-research-concepts.pdf.Google Scholar
Aufrère, 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: 13311339.CrossRefGoogle ScholarPubMed
Badoux, S (1965) Etude des caracteres morphologiques, physiologiques et agronomiques de populations d'esparcette (Onobrychis spp.). Recherche Agronomique Suisse 4: 111190.Google Scholar
Baimiev, AK, Baimiev, AK, Gubaidullin, II, Kulikovo, OL and Chemeris, AV (2007) Bacteria closely related to Phyllobacterium trifolii according to their 16S rRNA gene are discovered in the nodules of Hungarian sainfoin. Russian Journal of Genetics 43: 587590.CrossRefGoogle ScholarPubMed
Barea, JM and Azcon-Aguilar, C (1983) Mycorrhizas and their significance in nodulating nitrogen-fixing plants. Advances in Agronomy 36: 154.CrossRefGoogle Scholar
Barea, JM, Azconaguilar, C and Azcon, R (1987) Vesicular-arbuscular mycorrhiza improve both symbiotic N2 fixation and N uptake from soil as assessed with a N15 technique under field conditions. New Phytologist 106: 717725.CrossRefGoogle 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
Bate-Smith, EC (1975) Phytochemistry of proanthocyanidins. Phytochemistry 14: 11071113.CrossRefGoogle Scholar
Berard, NC, Holley, RA, McAllister, TA, Ominski, KH, Wittenberg, KM, Bouchard, KS, Bouchard, JJ and Krause, DO (2009) Potential to reduce Escherichia coli shedding in cattle feces by using sainfoin (Onobrychis viciifolia) forage, tested in vitro and in vivo. Applied and Environmental Microbiology 75: 10741079.CrossRefGoogle ScholarPubMed
Bermingham, EN, Hutchinson, KJ, Revell, DK, Brookes, IM and McNabb, WC (2001) The effect of condensed tannins in sainfoin (Onobrychis viciifolia) and sulla (Hedysarum coronarium) on digestion of amino acids in sheep. Proceedings of the New Zealand Society of Animal Production 61: 116119.Google Scholar
Biesmeijer, JC, Roberts, SP, Reemer, M, Ohlemueller, R, Edwards, M, Peeters, T, Schaffers, A, Potts, SG, Kleukers, R, Thomas, CD, Settele, J and Kunin, WE (2006) Parallel declines in pollinators and insect-pollinated plants in Britain and the Netherlands. Science 313: 351354.CrossRefGoogle ScholarPubMed
Bland, BF (1971) Crop Production: Cereals and Legumes. Academic Press: London UK, pp. 431444.Google Scholar
Borreani, G, Peiretti, PG and Tabacco, E (2003) Evolution of yield and quality of sainfoin (Onobrychis viciifolia Scop.) in the spring growth cycle. Agronomie 23: 193201.CrossRefGoogle Scholar
Burton, JC and Curley, RL (1968) Nodulation and nitrogen fixation in sainfoin (Onobrychis sativa LAM.) as influenced by strains of rhizobia. Sainfoin Symposium: 35.Google Scholar
Carleton, AE and Wiesner, LE (1968) Production of sainfoin seed. Sainfoin Symposium, Montana State University, December 12–13 1968.Google Scholar
Celiktas, N, Can, E, Hatipoglu, R and Avci, S (2006) Somatic embryogenesis, callus production, and plantlet growth in sainfoin (Onobrychis viciifolia Scop.). New Zealand Journal of Agricultural Research 49: 383388.CrossRefGoogle Scholar
Chen, B (1992) Sainfoin. In: Lanzhou, (ed.) Gansun Sci-tech Press: P. R. China, p. 20.Google Scholar
Clarke, PJ, Davison, EA and Fulloon, L (2000) Germination and dormancy of grassy woodland and forest species: effects of smoke, heat, darkness and cold. Australian Journal of Botany 48: 687699.CrossRefGoogle Scholar
Clement, SL, Griswold, TL, Rust, RW, Hellier, BC and Stout, DM (2006) Bee associates of flowering Astragalus and Onobrychis genebank accessions at a Snake River site in Eastern Washington. Journal of the Kansas Entomological Society 79: 254260.CrossRefGoogle Scholar
Cooper, CS (1972) Establishment, hay yield, and persistence of two sainfoin growth types seeded alone and with low growing grasses and legumes. Agronomy Journal 64: 379381.Google Scholar
Cox-Foster, DL, Conlan, S, Holmes, EC, Palacios, G, Evans, JD, Moran, NA, Quan, P, Briese, T, Hornig, M, Geiser, DM, Martinson, V, vanEngelsdorp, D, Kalkstein, AL, Drysdale, A, Hui, J, Zhai, J, Cui, L, Hutchison, SK, Simons, JF, Egholm, M, Pettis, JS and Lipkin, WI (2007) A metagenomic survey of microbes in honey bee colony collapse disorder. Science 318: 283287.CrossRefGoogle ScholarPubMed
Czochanska, Z, Foo, LY, Newman, RH and Porter, LJ (1980) Polymeric proanthocyanidins. Stereochemistry, structural units, and molecular weight. Journal of the Chemical Society, Perkin Transactions I: 22782286.CrossRefGoogle Scholar
Dewick, PM (1977) Biosynthesis of pterocarpan phtyoalexins in Trifolium pratense. Phytochemistry 16: 9397.CrossRefGoogle Scholar
Doyle, CJ, Thomson, DJ and Sheehy, JE (1984) The future of sainfoin in british agriculture – an economic assessment. Grass and Forage Science 39: 4351.CrossRefGoogle Scholar
Dubbs, AL (1968) The performance of sainfoin and sainfoin-grass mixture on dryland in central Montana. Sainfoin symposium; 1968 December 12-13, Bozeman, MT: Montana Agricultural Experiment Station Bulletin 627: 2225.Google Scholar
Egan, AR and Ulyatt, MJ (1980) Quantitative digestion of fresh herbage by sheep. VI. Utilization of nitrogen in five herbages. Journal of Agricultural Science 94: 4756.CrossRefGoogle Scholar
Eischen, FA, Graham, RH and Rivera, R (2009) Optimum time for feeding protein to wintering honey bee colonies in preparation for almond pollination. Proceedings of the American Bee Research Conference, 4–6 February, 2009, Gainesville, FL 2009 587.Google Scholar
Eken, C, Demirci, E and Dane, E (2004) Species of Fusarium on sainfoin in Erzurum, Turkey. New Zealand Journal of Agricultural Research 47: 261263.CrossRefGoogle Scholar
Emre, I, Turgut-balik, D, Sahin, A and Kursat, M (2007) Total electrophoretic band patterns of some Onobrychis species growing in Turkey. American-Eurasian Journal of Agricultural and Environmental Sciences 2: 123126.Google Scholar
Frame, J, Charlton, JFL and Laidlaw, AS (1998) Temperate forage legumes. CAB International.Google Scholar
Fraser, MD, Fychan, R and Jones, R (2000) Voluntary intake, digestibility and nitrogen utilization by sheep fed ensiled forage legumes. Grass Forage Science 55: 271279.CrossRefGoogle Scholar
Gea, A, Stringano, E, Brown, RH and Mueller-Harvey, I (2011) In situ analysis and structural elucidation of sainfoin (Onobrychis viciifolia) tannins for high throughput germplasm screening. Journal of Agricultural and Food Chemistry (doi:http://pubs.acs.org/doi/abs/10.1021/jf103609p ).CrossRefGoogle ScholarPubMed
Givens, DI and Rulquin, H (2004) Utilisation by ruminants of nitrogen compounds in silage-based diets. Animal Feed Science and Technology 114: 118.Google Scholar
Givens, DI and Shingfield, KJ (2004) Foods derived from animals: the impact of animal nutrition on their nutritive value and ability to sustain long-term health. Nutrition Bulletin 29: 325332.CrossRefGoogle Scholar
Goplen, BP, Richards, KW and Moyer, JR (1991) Sainfoin for Western Canada, Agriculture Canada Publication 1470/E.Google Scholar
Gray, FA, Shigaki, T, Koch, DW, Delaney, RD, Gray, AM, Majerus, ME, Cash, D, Ditterline, RL and Wichman, DM (2006) Registration of ‘Shoshone’ Sainfoin. Crop Science 46: 988.CrossRefGoogle Scholar
Grabber, J, Broderick, G, Russelle, M, Powell, M, Rotz, A, Muck, R, Mertens, D and Massingill, L (2002) Tannin-containing forage crops: a way to improve nitrogen use and profitability of dairy farms? http://www.dfrc.ars.usda.gov/cd/posters/Tannin%20dafosym.pdf.Google Scholar
Guner, A, Ozhatay, N, Ekim, T and Baser, K (2000) Flora of Turkey and East Aegean Islands. In: Press, EU (ed.) vol. 11, pp. 9899.Google Scholar
Hanley, ME, Franco, M, Pichon, S, Darvill, B and Goulson, D (2008) Breeding system, pollinator choice and variation in pollen quality in British herbaceous plants. Functional Ecology 22: 592598.CrossRefGoogle Scholar
Häring, DA, Scharenberg, A, Heckendorn, F, Dohme, F, Lüscher, A, Maurer, V, Suter, D and Hertzberg, H (2008) Tanniferous forage plants: agronomic performance, palatability and efficacy against parasitic nematodes in sheep. Renewable Agriculture and Food Systems 23: 1929.CrossRefGoogle Scholar
Harrison, MJ (1998) Development of the arbuscular mycorrhizal symbiosis. Current Opinion in Plant Biology 1: 360365.CrossRefGoogle ScholarPubMed
Hart, SP and Sahlu, T (1993) Mohair production and body-weight gains of yearling Angora goats grazing forages with different tannin levels. Proceedings of XVII International Grassland Congress, Palmerston North, New Zealand. 575.Google Scholar
Hartlib, S (1652) His legacy.Google Scholar
Hartwig, UA and Nosberger, J (1996) Symbiotic nitrogen fixation: a physiological link between plant and environment. In: Younie, D (ed.) Legumes in Sustainable Farming Systems. Occasional Symposium no. 30. British Grassland Society. pp. 3643.Google Scholar
Haynes, RJ (1980) Competitive aspects of the grass-legume association 227-256. In: Brady, NC (ed.) Advances in Agronomy. 33 New York: Academic Press. ISBN 0-12-000 733-39.Google 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
Hendrikx, P, Chauzat, M-P, Debin, M, Neuman, P, Fries, I, Ritter, W, Brown, M, Mutinelli, F, Le Conte, Y and Gregorc, A (2009) Bee mortality and bee surveillance in Europe. Scientific report submitted to EFSA. CFP/EFSA/AMU/2008/02. Published 3 December 2009.Google Scholar
Hill, R (1997) Sainfoin: the not quite forgotten legume. In: Lane, GPF and Wilkinson, JM (eds) Alternative Forages for Ruminants. Papers, Conference, Cirencester, pp. 5559.Google Scholar
Horne, M (1995) Pollen preference and its relationship to nesting success of Megachile rotundata (Hymenoptera, Megachilidae). Annals of the Entomological Society of America 88: 862867.CrossRefGoogle Scholar
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
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.Google ScholarPubMed
Howes, FN (2007) ‘Plants and Beekeeping’. London: Faber & Faber, p. 260.Google Scholar
Hughes, SJ (1949) Studies on some diseases of sainfoin (Onobrychis sativa) II. The life history of Ramularia onobrychidis Allescher. Transactions British Mycological Society 32: 3459.CrossRefGoogle Scholar
Hutchinson, JB (1965) Crop Plant Evolution: A General Discussion. Essays on Crop Plant Evolution. London: Cambridges University Press, pp. 166181.Google Scholar
Ingham, JL (1978) Flavonoid and isoflavonoid compounds from leaves of sainfoin (Onobrychis viciifolia). Zeitschrift fuer Naturforschung 33c: 146148.CrossRefGoogle Scholar
John, A and Lancashire, JA (1981) Aspects of the feeding and nutritive value of Lotus species. Proceedings of the New Zealand Grasslands Association 42: 152159.CrossRefGoogle Scholar
Jones, GA, McAllister, TA, Muir, AD and Cheng, KJ (1994) Effects of sainfoin (Onobrychis viciifolia Scop.) condensed tannins on growth and proteolysis by four strains of ruminal bacteria. Applied and Environmental Microbiology 60: 13741378.CrossRefGoogle ScholarPubMed
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, Broadhurst, RB and Lyttleton, JW (1976) The condensed tannins of pasture legume species. Phytochemistry 15: 14071409.CrossRefGoogle Scholar
Karnezos, TP, Matches, AG and Brown, CP (1994) Spring lamb production on alfalfa, sainfoin, and wheatgrass pastures. Agronomy Journal 86: 497502.CrossRefGoogle Scholar
Kells, A (2001) Sainfoin: an alternative forage crop for bees. Bee World 82: 192194.CrossRefGoogle Scholar
Kidambi, SP, Mahan, JR and Matches, AG (1990) Purification and thermal dependence of glutathione reductase from two forage legume species. Plant Physiology 92: 363367.CrossRefGoogle ScholarPubMed
Kingston-Smith, AH, Bollard, AL, Shaw, RK, Davies, TE and Theodorou, MK (2003) Correlations between protein content and protease activity in forage crops. Aspects of Applied Biology 70: 101105.Google Scholar
Koivisto, JM and Lane, GPF (2001) Sainfoin Worth Anothe Look. http://www.fao.org/AG/AGp/agpc/doc/Gbase/AddInfo/sainfoin.pdf.Google Scholar
Koter, Z (1965) Nutrition of Leguminous plants. 1. The effect of different forms of N on the growth and symbiotic N2-fixation by red clover and sainfoin plants. 2. The effect of increasing amount of N on the yield and N2-fixation by Sainfoin (Onobrychis viciifolia var. persica). Pamielnik pulawski 20: 337.Google Scholar
Koupai-Abyazani, M, McCallum, J and Bohm, BA (1992) Identification of the constituent flavanoid units in sainfoin proanthocyanidins by reversed-phase high-performance liquid chromatography. Journal of Chromatography 594: 117123.CrossRefGoogle Scholar
Koupai-Abyazani, M, Muir, AD, Bohm, BA, Towers, GHN and Gruber, MY (1993a) The proanthocyanidin polymers in some species of Onobrychis. Phytochemistry 34: 113117.CrossRefGoogle Scholar
Koupai-Abyazani, M, McCallum, J, Muir, AD, Bohm, BA, Towers, GHN and Gruber, MY (1993b) Developmental changes in the composition of proanthocyanidins from leaves of sainfoin (Onobrychis viciifolia Scop.) as determined by HPLC anlaysis. Journal of Agricultural and Food Chemistry 41: 10661070.CrossRefGoogle Scholar
Lees, GL, Suttill, NH and Gruber, MY (1993) Condensed tannins in sainfoin. 1. A histological and cytological survey of plant tissues. Canadian Journal of Botany 71: 11471152.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.Google Scholar
Liu, Z (2006) Developing a modern agronomy for sainfoin (Onobrychis viciifolia Scop.). PhD Thesis, Coventry University in association with Royal Agricultural College.Google Scholar
Liu, Z, Lane, GPF and Davies, WP (2006) The effects of establishment method on the yield of sainfoin (Onobrychis viciifolia) and sainfoin–grass mixtures. Proceedings of British Grassland Society 8th Research Conference.Google Scholar
Lu, Y, Sun, Y, Foo, LY, McNabb, WC and Molan, AL (2000) Phenolic glycosides of forage legume Onobrychis viciifolia. Phytochemistry 55: 6775.Google Scholar
MAAREC (2006) Mid-Atlantic Apiculture Research and Extension Consortium (MAAREC) – CCD Working Group. Colony Collapse Disorder Preliminary Report, p. 22.Google Scholar
Manning, R (2001) Fatty acids in pollen: a review of their importance for honey bees. Bee World 82: 6075.CrossRefGoogle Scholar
Manning, R (2006) Fatty acid composition of pollen and the effect of two dominant fatty acids (linoleic and oleic) in pollen and flour diets on longevity and nutritional composition of honey bees (Apis mellifera). PhD Thesis, Murdoch University.Google Scholar
Marais, JPJ, Mueller-Harvey, I, Brandt, EV and Ferreira, D (2000) Polyphenols, condensed tannins and other natural products in Onobrychis viciifolia (Sainfoin). Journal of Agricultural and Food Chemistry 48: 34403447.CrossRefGoogle ScholarPubMed
Marten, GC, Ehle, FR and Ristau, EA (1987) Performance and photosensitization of cattle related to forage quality of four legumes. Crop Science 27: 138145.CrossRefGoogle Scholar
Martiniello, P (2005) Recurrent phenotypic selection of legumes and grass perennial forage crops using Mediterranean autochthonous germplasm. Journal of Genetics and Breeding 59: 34.Google Scholar
Mathre, D (1968) Disease in sainfoin. Sainfoin Symposium: 6566.Google Scholar
McAllister, TA, Martinez, T, Bae, HD, Muir, AD, Yanke, LJ and Jones, GA (2005) Characterization of condensed tannins purified from legume forages: chromophore production, protein precipitation, and inhibitory effects on cellulose digestion. Journal of Chemical Ecology 31: 20492067.CrossRefGoogle ScholarPubMed
McGregor, SE (1976) Insect pollination of cultivated crop plants, Chapter 4 in ‘Legumes and Some Relatives’. Available at http://gears.tucson.ars.ag.gov/book/.Google Scholar
McMahon, LR, McAllister, TA, Berg, BP, Majak, W, Acharya, SN, Popp, JD, Coulman, BE, Wang, Y and Chen, K-J (2000) A review of the effects of forage condensed tannins on ruminal fermentation and bloat in grazing cattle. Canadian Journal of Plant Science 80: 469485.CrossRefGoogle Scholar
Meyer, DW (1975) Yield, regrowth and persistence of sainfoin under fertilisation. Agronomy Journal 67: 439441.CrossRefGoogle Scholar
Meyer, DW and Badaruddin, M (2001) Frost tolerance of ten seedling legume species at four growth stages. Crop Science 41: 18381842.CrossRefGoogle Scholar
Min, BR, Barry, TN, Attwood, GT and 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: 319.CrossRefGoogle Scholar
Min, BR, McNabb, WC, Barry, TN and Peters, JS (2000) Solubilization and degradation of ribulose-1,5-bisphosphate carboxylase/oxygenase (EC 4.1.1.39; Rubisco) protein from white clover (Trifolium repens) and Lotus corniculatus by rumen microorganisms and the effect of condensed tannins on these processes. Journal of Agricultural Science (Cambridge) 134: 305317.CrossRefGoogle Scholar
Molle, G, Decandia, M, Soelter, U, Greef, JM, Rochon, JJ, Sitzia, M, Hopkins, An and Rook, AJ (2008) The effect of different legume-based swards on intake and performance of pgrazing ruminants under Mediterranean and cool temperate conditions. Grass and Forage Science 63: 513530.CrossRefGoogle Scholar
Morrill, WL, Ditterline, RL and Cash, SD (1998) Insect pests and associated root pathogens of sainfoin in western USA. Field Crops Research 59: 129134.CrossRefGoogle Scholar
Moyer, JR (1985) Effect of weed control and a companion crop on alfalfa and sainfoin establishment, yields and nutrient composition. Canada Journal of Plant Science 65: 107116.CrossRefGoogle Scholar
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 (2009) ‘Holy hay’ – re-inventing a traditional animal feed. Biologist 56: 2227.Google Scholar
Mueller-Harvey, I and Dhanoa, MS (1991) Varietal differences among sorghum crop residues in relation to their phenolic HPLC fingerprints and responses to different environments. Journal of the Science of Food and Agriculture 57: 199216.CrossRefGoogle Scholar
Negri, V and Cenci, CA (1988) Morphological characterization of natural populations of Onobrychis viciifolia (Leguminosae) from Central Italy. Willdenowia 17: 1931.Google Scholar
Negri, V, Veronesi, F and Falcinelli, M (1987) Germplasm evaluation of Onobrychis viciifolia Scop. for agronomic traits. Genetica Agraria.Google Scholar
Newman, G (1997) An overview of forage legumes. In: Lane, GPF and Wilkinson, JM (eds) Alternative Forages for Ruminants. Cirencester, UK, pp. 314.Google Scholar
Ojeda-Robertos, N, Manolaraki, F, Theodoridou, K, Aufrere, J, Halbwirth, H, Stich, K, Regos, I, Treutter, D, Mueller-Harvey, I and Hoste, H (2010) The anthelmintic effect of sainfoin (silage, hay, fresh) and the role of flavonoid glycosides. 61st Annual Meeting, European Association of Animal Production, Heraklion, Crete, Greece. 23–27 August 2010.Google Scholar
Paolini, V, De La Farge, F, Prevot, F, Dorchies, PH and Hoste, H (2005) Effects of the repeated distribution of sainfoin hay on the resistance and the resilience of goats naturally infected with gastrointestinal nematodes. Veterinary Parasitology 127: 277283.CrossRefGoogle ScholarPubMed
Parker, RJ and Moss, BR (1981) Nutritional value of sainfoin hay compared with alfalfa hay. Journal of Dairy Science 64: 206210.CrossRefGoogle Scholar
Pecetti, L, Annicchiarico, P, Battini, F and Cappelli, S (2009) Adaptation of forage legume species and cultivars under grazing in two extensive livestock systems in Italy. European Journal of Agronomy 30: 199204.CrossRefGoogle Scholar
Piper, CV (1924) Forage Plants and their Culture. New York: The Macmillan Co.Google Scholar
Potts, SG, Roberts, SPM, Dean, R, Marris, G, Brown, M, Jones, R and Settele, J (2010) Declines of managed honeybees and beekeepers in Europe. Journal of Apicultural Research 49: 1522.Google Scholar
Prévost, D, Bordeleau, LM and Antoun, H (1987) Symbiotic effectiveness of indigenous arctic rhizobia on temperate forage legume – sainfoin (Onobrychis viciifolia). Plant and Soil 104: 6369.CrossRefGoogle Scholar
Provorov, NA and Tikhonovich, IA (2003) Genetic resources for improving nitrogen fixation in legume-rhizobia symbiosis. Genetic resources and Crop Evoloutuion 50: 8999.CrossRefGoogle Scholar
Regos, I, Urbanella, A and Treutter, D (2009) Idenficiation and quantification of phenolic compounds from the forage legume sainfoin (Onobrychis viciifolia). Journal of Agricultural Food and Chemistry 57: 58435852.CrossRefGoogle ScholarPubMed
Rios-de Álvarez, L, Greer, AW, Jackson, F, Athanadiadou, S, Kyriazakis, I and Huntley, JF (2008) The effect of dietary sinafoin (Onobrychis viciifolia) on local cellular responses to Trichostrongylus colubriformis in sheep. Parasitology 135: 1171124.CrossRefGoogle ScholarPubMed
Rochon, JJ, Doyle, CJ, Greef, JM, Hopkins, A, Molle, G, Sitzia, M, Scholefield, D and Smith, CJ (2004) Grazing legumes in Europe: a review of their status, management, benefits, research needs and future prospects. Grass and Forage Science 59: 197214.CrossRefGoogle Scholar
Rosov, SA (1952) Sainfoin - one of the best honey plants in crop rotation. Pchelovodstvo Mosk 29: 4652.Google Scholar
Rozen, JG, Ozebek, H, Ascher, JS, Sedivy, C, Praz, C, Monfared, A and Mueller, A (2010) Nests, petal usages, floral preferences, and immatures of Osmia (Ozbekosmia) avosetta (Megachilidae: Megachilinae: Osmiini), including biological comparisons with other Osmiine bees. American Museum Novitates 3680: 122.CrossRefGoogle Scholar
Rumball, W and Claydon, RB (2005) Germplasm release – ’G35’ Sainfoin (Onobrychis viciifolia Scop.). New Zealand Journal of Agricultural Research 48: 127128.CrossRefGoogle Scholar
Russell, GB, Shaw, GJ, Christmas, PE, Yates, MB and Sutherland, RW (1984) Two 2-arylbenzofurans as insect feeding deterrents from sainfoin (Onobrychis viciifolia). Phytochemistry 23: 14171420.CrossRefGoogle Scholar
Sánchez-Yélamo, MD (2006) Rapid characterisation of some species of the genus Onobrychis Miller (Leguminosae: Papilionoideae) by isozyme methods. Seed Science and Technology 34: 297306.Google Scholar
Scharenberg, A, Arrigo, Y, Gutzwiller, A, Wyss, U, Hess, HD, Kreuzer, M and Dohme, F (2007) Effect of feeding dehydrated and ensiled tanniferous sainfoin (Onobrychis viciifolia) on nitrogen and mineral digestion and metabolism of lambs. Archives of Animal Nutrition 61: 390405.Google ScholarPubMed
Scharenberg, A, Heckendorn, F, Arrigo, Y, Hertzberg, H, Gutzwiller, A, Hess, HD, Kreuzer, M and Dohme, F (2008) Nitrogen and mineral balance of lambs artificially infected with Haemonchus contortus and fed tanniferous sainfoin (Onobrychis viciifolia). Journal of Animal Science 86: 18791890.Google ScholarPubMed
Shan, MH, Singh, KN, Kachroo, D and Khanday, BA (1991) Performance of lucerne and sainfoin under different cuttings and levels of phosphorus. Indian Journal of Agronomy 36: 6166.Google Scholar
Shaw, AL (1968) The certification program for sainfoin in Montana. Sainfoin Symposium Montana. Agricultural Experiment Station Bulletin: 7778.Google Scholar
Sheehy, JE, Minchin, FR and McNeill, A (1984) Physiological principles governing the growth and development of lucerne, sainfoin and red clover. In Forage Legumes. Proceedings of a Symposium, February 21–23, 1984. British Grassland Society, pp. 113125.Google Scholar
Sheehy, JE and Popple, SC (1981) Photosynthesis, water relations, temperature and canopy structure as factors influencing the growth of sainfoin (Onobrychis viciifolia Scop.) and Lucerne (Medicago sativa L.). Annals of Botany 48: 113128.CrossRefGoogle Scholar
Sheldrick, R, Thomson, D and Newman, G (1987) Sainfoin. In: Legumes for Milk and Meat. Chalcombe Publications: Marlow, UK, pp. 5969.Google Scholar
Sheldrick, RD and Thomson, DJ (1982) Management and Utilization of Sainfoin (Onobrychis Sativa) Information Leaflet no. 13.Google Scholar
Sims, JR, Muir, MK and Carleton, AE (1968) Evidence of ineffective rhizobia and its relation to the nitrogen nutrition of sainfoin (Onobrychis viciaefolia). Sainfoin Symposium Montana. Agricultural Experiment Station Bulletin 627: 812.Google Scholar
Širjaev, G (1925) Onobrychis generis revisio critica. Brno.Google Scholar
Sprent, J (2003) Plant biology: Mutual sanctions. Nature 422: 672674.CrossRefGoogle ScholarPubMed
Stewart, JL, Mould, F and Mueller-Harvey, I (2000) The effect of drying treatment on the fodder quality and tannin content of two provenances of Calliandra calothyrsus Meissner. Journal of the Science of Food and Agriculture 80: 14611468.3.0.CO;2-R>CrossRefGoogle Scholar
Stringano, E, Hayot, C, Smith, L, Theodoridou, K, Aufrére, J, Brown, RH, Hayes, W, Cramer, R and Mueller-Harvey, I (2010) Thiolytic screening method for exploring condensed tannin variation in a unique sainfoin germplasm bank. 58th International Congress and Annual Meeting of the Society of Medicinal Plant and Natural Product Research and 7th Tannin Conference, 29th Aug- 2th Sep 2010. Berlin, Germany. Planta Medica 76: 1166.Google Scholar
Syngenta (2008) Ensuring there is honey still for tea. http://www.syngenta.com/en/features/honey_tea.htm.Google Scholar
Taki, H, Okabe, K, Makino, S, Yamaura, Y and Sueyoshi, M (2009) Contribution of small insects to pollination of common buckwheat, a distylous crop. Annals of Applied Biology 155: 121129.CrossRefGoogle Scholar
Tamas, E (2006) Citological aspects of the Onobrychis genus. Bulletin of University of Agricultural Sciences and Veterinary Medicine Cluj-Napoca. Agriculture 62: 154158.Google Scholar
Tamminga, S (1992) Nutrition management of dairy cows as a contribution to pollution control. Journal of Dairy Science 75: 345357.CrossRefGoogle Scholar
Tamminga, S, Bannink, A, Kijkstra, J and Zom, R (2007) Feeding strategies to reduce methane loss in cattle. Report 34. Animal Sciences Group, Wageningen University, The Netherlands. p. 44 http://www2.asg.wur.nl/NR/rdonlyres/F81D8745-6596-4296-A292-8553950E2B98/42707/34.pdf (checked on 20 April 2010).Google Scholar
Tasei, JN (1984) Forage and protein legumes. In: Pesson, PL (ed.) Pollination and Plant Productions. Paris: INRA, pp. 261308.Google Scholar
Tasei, JN and Aupinel, P (2008) Nutritive value of 15 single pollens and pollen mixes tested on larvae produced by bumblebee workers (Bombus terrestris, Hymenoptera: Apidae). Apidologie 39: 397409.CrossRefGoogle Scholar
Theodoridou, K, Aufrère, J, Andueza, D, Pourrat, J, Le Morvan, A, Stringano, E, Mueller-Harvey, I and Baumont, R (2010) Effects of condensed tannins in fresh sainfoin (Onobrychis viciifolia) on in vivo and in situ digestion in sheep. Animal Feed Science and Technology 160: 2338.Google Scholar
Thomson, DJ (1982) Nutritive and utilisation value of sainfoin. In: The Future of Sainfoin in British Agriculture. Hurley: The Grassland Research Institute, pp. 811.Google Scholar
Thomson, DJ, Beever, DE, Harrison, DG, Hill, IW and Osbourn, DF (1971) The digestion of dried lucerne (Medicago sativa, L.) and dried sainfoin (Onobrychis viciifolia, Scop.) by sheep. Proceedings of the Nutrition Society 30: 14A.Google ScholarPubMed
Thomson, JR (1951a) Sainfoin in its first harvest year. Journal of British Grassland Society 6: 107117.Google Scholar
Thomson, JR (1951b) Seed studies in sainfoin. Journal of British Grassland Society 6: 147159.Google Scholar
Thomson, JR (1952) Further seed studies in sainfoin. Grass and Forage Science 7: 6569.CrossRefGoogle Scholar
Tufenkci, S, Erman, M and Sonmez, F (2006) Effects of phosphorus and nitrogen applications and Rhizobium inoculation on the yield and nutrient uptake of sainfoin (Onobrychis viciifolia L.) under irrigated conditions in Turkey. New Zealand Journal of Agricultural Research 49: 101105.CrossRefGoogle Scholar
USDA SARE (2007) Managing Cover Crops Profitably, 3rd edn. http://www.sare.org/publications/covercrops/buckwheat.shtml, p. 244.Google Scholar
Van Engelsdorp, D, Underwood, R, Caron, D and Hayes, J Jr (2007) An estimate of managed colony losses in the winter of 2006–2007: a report commissioned by the apiary inspectors of America. American Bee Journal 147: 599603.Google Scholar
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: 116139.Google Scholar
Waghorn, GC, Jones, WT, Shelton, ID and McNabb, WC (1990) Condensed tannins and the nutritive value of herbage. Proceedings of the New Zealand Grasslands Association 51: 171176.Google Scholar
Waghorn, GC and McNabb, WC (2003) Consequences of plant phenolic compounds for productivity and health of ruminants. Proceedings of the Nutrition Society 62: 383392.Google ScholarPubMed
Wallace, LE (1968) Current and potential insect problems of sainfoin in America. Sainfoin Symposium Montana. Agricultural Experiment Station Bulletin 627: 6770.Google Scholar
Waller, PJ (2006) From discovery to development: current industry perspectives for the development of novel methods of helminth control in livestock. Veterinary Parasitology 139: 114.Google ScholarPubMed
Wang, Y, Barbieri, LR, Berg, BP and McAllister, TA (2007) Effects of mixing sainfoin with alfalfa on ensiling, ruminal fermentation and total tract digestion of silage. Animal Feed Science and Technology 135: 296314.CrossRefGoogle Scholar
Wang, Y, Berg, BP, Barbieri, LR, Veira, DM and McAllister, TA (2006) Comparison of alfalfa and mixed alfalfa-sainfoin pastures for grazing cattle: effects on incidence of bloat, ruminal fermentation, and feed intake. Canadian Journal of Animal Science 86: 383392.CrossRefGoogle Scholar
Westphal, C, Bommarco, R, Lamborn, E, Petanidou, T, Potts, SG, Roberts, SPM, Szentgyörgyi, H, Vaissière, BE, Woyciechowski, M and Steffan-Dewenter, I (2008) Measuring bee biodiversity in different habitats and biogeographic regions. Ecological Monographs 78: 653671.CrossRefGoogle Scholar
Wiesner, LE, Carleton, AE and Cooper, CS (1968) Factors affecting sainfoin seed germination and emergence. Sainfoin Symposium Montana. Agricultural Experiment Station Bulletin: 1315.Google Scholar
Williams, PH and Osborne, JL (2009) Bumblebee vulnerability and conservation world-wide. Apidologie 40: 367387.CrossRefGoogle Scholar
Yildiz, B, Ciplak, B and Aktoklu, E (1999) Fruit morphology of sections of the genus Onobrychis Miller (Fabaceae) and its phylogenetic implications. Israel Journal of Plant Sciences 47: 269282.Google Scholar