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Structural features of condensed tannins affect in vitro ruminal methane production and fermentation characteristics

Published online by Cambridge University Press:  16 August 2016

N. T. HUYEN ,
C. FRYGANAS ,
G. UITTENBOGAARD ,
I. MUELLER-HARVEY ,
M. W. A. VERSTEGEN ,
W. H. HENDRIKS  and
W. F. PELLIKAAN
N. T. HUYEN*
Affiliation:
Animal Nutrition Group, Department of Animal Sciences, Wageningen University, PO Box 338, 6700 AH Wageningen, the Netherlands
C. FRYGANAS
Affiliation:
Chemistry & Biochemistry Laboratory, School of Agriculture, Policy and Development, University of Reading, PO Box 236, 1 Earley Gate, Reading RG6 6AT, UK
G. UITTENBOGAARD
Affiliation:
Animal Nutrition Group, Department of Animal Sciences, Wageningen University, PO Box 338, 6700 AH Wageningen, the Netherlands
I. MUELLER-HARVEY
Affiliation:
Chemistry & Biochemistry Laboratory, School of Agriculture, Policy and Development, University of Reading, PO Box 236, 1 Earley Gate, Reading RG6 6AT, UK
M. W. A. VERSTEGEN
Affiliation:
Animal Nutrition Group, Department of Animal Sciences, Wageningen University, PO Box 338, 6700 AH Wageningen, the Netherlands
W. H. HENDRIKS
Affiliation:
Animal Nutrition Group, Department of Animal Sciences, Wageningen University, PO Box 338, 6700 AH Wageningen, the Netherlands Department of Farm Animal Health, Faculty of Veterinary Medicine, Utrecht University, PO Box 80·163, 3508 TD Utrecht, the Netherlands
W. F. PELLIKAAN
Affiliation:
Animal Nutrition Group, Department of Animal Sciences, Wageningen University, PO Box 338, 6700 AH Wageningen, the Netherlands
*
*To whom all correspondence should be addressed. Email: [email protected]
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Summary

An in vitro study was conducted to investigate the effects of condensed tannin (CT) structural properties, i.e. average polymer size (or mean degree of polymerization), percentage of cis flavan-3-ols and percentage of prodelphinidins in CT extracts on methane (CH4) production and fermentation characteristics. Condensed tannins were extracted from eight plants in order to obtain different CT types: blackcurrant leaves, goat willow leaves, goat willow twigs, pine bark, redcurrant leaves, sainfoin plants, weeping willow catkins and white clover flowers. They were analysed for CT content and CT composition by thiolytic degradation, followed by high performance liquid chromatography (HPLC) analysis. Grass silage was used as a control substrate. Condensed tannins were added to the substrate at a concentration of 40 g/kg, with or without polyethylene glycol (+ or −PEG 6000 treatment) to inactivate tannins, then incubated for 72 h in mixed buffered rumen fluid from three different lactating dairy cows per run. Total cumulative gas production (GP) was measured by an automated GP system. During the incubation, 12 gas samples (10 µl) were collected from each bottle headspace at 0, 2, 4, 6, 8, 12, 24, 30, 36, 48, 56 and 72 h of incubation and analysed for CH4. A modified Michaelis-Menten model was fitted to the CH4 concentration patterns and model estimates were used to calculate total cumulative CH4 production (GPCH4). Total cumulative GP and GPCH4 curves were fitted using biphasic and monophasic modified Michaelis-Menten models, respectively. Addition of PEG increased GP, GPCH4, and CH4 concentration compared with the −PEG treatment. All CT types reduced GPCH4 and CH4 concentration. All CT increased the half time of GP and GPCH4. Moreover, all CT decreased the maximum rate of fermentation for GPCH4 and rate of substrate degradation. The correlation between CT structure and GPCH4 and fermentation characteristics showed that the proportion of prodelphinidins within CT had the largest effect on fermentation characteristics, followed by average polymer size and percentage of cis flavan-3-ols.

Type
Animal Research Papers
Information
The Journal of Agricultural Science , Volume 154 , Issue 8 , November 2016 , pp. 1474 - 1487
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Copyright
Copyright © Cambridge University Press 2016 

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References

Alexander, G., Singh, B., Sahoo, A. & Bhat, T. K. (2008). In vitro screening of plant extracts to enhance the efficiency of utilization of energy and nitrogen in ruminant diets. Animal Feed Science and Technology 145, 229–244.Google Scholar
Bauer, E., Williams, B. A., Voigt, C., Mosenthin, R. & 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.Google Scholar
Beauchemin, K. A., McGinn, S. M., Martinez, T. F. & McAllister, T. A. (2007). Use of condensed tannin extract from quebracho trees to reduce methane emissions from cattle. Journal of Animal Science 85, 1990–1996.Google Scholar
Beauchemin, K. A., McAllister, T. A. & McGinn, S. M. (2009). Dietary Mitigation of Enteric Methane from Cattle. CAB Reviews: Perspectives in Agriculture, Veterinary Science, Nutrition and Natural Resources 4, no. 035, 1–18. Wallingford, UK: CABI.CrossRefGoogle Scholar
Bhatta, R., Uyeno, Y., Tajima, K., Takenaka, A., Yabumoto, Y., Nonaka, I., Enishi, O. & Kurihara, M. (2009). Difference in the nature of tannins on in vitro ruminal methane and volatile fatty acid production and on methanogenic archaea and protozoal populations. Journal of Dairy Science 92, 5512–5522.Google Scholar
Bhatta, R., Saravanan, M., Baruah, L., Sampath, K. T. & Prasad, C. S. (2013). Effect of plant secondary compounds on in vitro methane, ammonia production and ruminal protozoa population. Journal of Applied Microbiology 115, 455–465.CrossRefGoogle ScholarPubMed
Boucher, O., Friedlingstein, P., Collins, B. & Shine, K. P. (2009). The indirect global warming potential and global temperature change potential due to methane oxidation. Environmental Research Letters 4, 044007. doi: 10.1088/1748-9326/4/4/044007 Google Scholar
Bunglavan, S. J. & Dutta, N. (2013). Use of tannins as organic protectants of proteins in digestion of ruminants. Journal of Livestock Science 4, 67–77.Google Scholar
Calabrò, S., Guglielmelli, A., Iannaccone, F., Danieli, P. P., Tudisco, R., Ruggiero, C., Piccolo, G., Cutrignelli, M. I. & Infascelli, F. (2012). Fermentation kinetics of sainfoin hay with and without PEG. Journal of Animal Physiology and Animal Nutrition 96, 842–849.CrossRefGoogle ScholarPubMed
Carulla, J. E., Kreuzer, M., Machmüller, A. & 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.CrossRefGoogle Scholar
Castillejos, L., Calsamiglia, S., Martín-Tereso, J. & Ter Wijlen, H. (2008). In vitro evaluation of effects of ten essential oils at three doses on ruminal fermentation of high concentrate feedlot-type diets. Animal Feed Science and Technology 145, 259–270.Google Scholar
Ellis, J. L., Dijkstra, J., Kebreab, E., Bannink, A., Odongo, N. E., McBride, B. W. & France, J. (2008). Aspects of rumen microbiology central to mechanistic modelling of methane production in cattle. Journal of Agricultural Science, Cambridge 146, 213–233.CrossRefGoogle Scholar
Gea, A., Stringano, E., Brown, R. H. & 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 59, 495–503.CrossRefGoogle ScholarPubMed
Getachew, G., Makkar, H. P. S. & Becker, K. (2000 a). Effect of polyethylene glycol on in vitro degradability of nitrogen and microbial protein synthesis from tannin-rich browse and herbaceous legumes. British Journal of Nutrition 84, 73–83.Google Scholar
Getachew, G., Makkar, H. P. S. & Becker, K. (2000 b). Tannins in tropical browses: effects on in vitro microbial fermentation and microbial protein synthesis in media containing different amounts of nitrogen. Journal of Agricultural and Food Chemistry 48, 3581–3588.Google Scholar
Getachew, G., Makkar, H. P. S. & Becker, K. (2002). Tropical browses: contents of phenolic compounds, in vitro gas production and stoichiometric relationship between short chain fatty acid and in vitro gas production. Journal of Agricultural Science, Cambridge 139, 341–352.Google Scholar
Grainger, C., Clarke, T., Auldist, M. J., Beauchemin, K. A., McGinn, S. M., Waghorn, G. C. & Eckard, R. J. (2009). Potential use of Acacia mearnsii condensed tannins to reduce methane emissions and nitrogen excretion from grazing dairy cows. Canadian Journal of Animal Science 89, 241–251.Google Scholar
Groot, J. C. J., Cone, J. W., Williams, B. A., Debersaques, F. M. A. & Lantinga, E. A. (1996). Multiphasic analysis of gas production kinetics for in vitro fermentation of ruminant feeds. Animal Feed Science and Technology 64, 77–89.Google Scholar
Hariadi, B. T. & Santoso, B. (2010). Evaluation of tropical plants containing tannin on in vitro methanogenesis and fermentation parameters using rumen fluid. Journal of the Science of Food and Agriculture 90, 456–461.Google Scholar
Hassanat, F. & Benchaar, C. (2013). Assessment of the effect of condensed (acacia and quebracho) and hydrolysable (chestnut and valonea) tannins on rumen fermentation and methane production in vitro . Journal of the Science of Food and Agriculture 93, 332–339.Google Scholar
Hatew, B., Hayot Carbonero, C., Stringano, E., Sales, L. F., Smith, L. M. J., Mueller-Harvey, I., Hendriks, W. H. & Pellikaan, W. F. (2015). Diversity of condensed tannin structures affects rumen in vitro methane production in sainfoin (Onobrychis viciifolia) accessions. Grass and Forage Science 70, 474–490.Google Scholar
Johnson, K. A. & Johnson, D. E. (1995). Methane emissions from cattle. Journal of Animal Science 73, 2483–2492.CrossRefGoogle ScholarPubMed
Jones, G. A., McAllister, T. A., Muir, A. D. & Cheng, K.-J. (1994). Effects of sainfoin (Onobrychis viciifolia Scop.) condensed tannins on growth and proteolysis by four strains of ruminal bacteria. Applied and Environmental Microbiology 60, 1374–1378.Google Scholar
Kumar, S., Choudhury, P. K., Carro, M. D., Griffith, G. W., Dagar, S. S., Puniya, M., Calabro, S., Ravella, S. R., Dhewa, T., Upadhyay, R. C., Sirohi, S. K., Kundu, S. S., Wanapat, M. & Puniya, A. K. (2014). New aspects and strategies for methane mitigation from ruminants. Applied Microbiology and Biotechnology 98, 31–44.Google Scholar
Makkar, H. P. S., Dawra, R. K. & Singh, B. (1988). Changes in tannin content, polymerisation and protein precipitation capacity in oak (Quercus incana) leaves with maturity. Journal of the Science of Food and Agriculture 44, 301–307.Google Scholar
Makkar, H. P. S., Blümmel, M. & Becker, K. (1995). Formation of complexes between polyvinyl pyrrolidones or polyethylene glycols and tannins, and their implication in gas production and true digestibility in in vitro techniques. British Journal of Nutrition 73, 897–913.Google Scholar
Marais, J. P. J., Mueller-Harvey, I., Brandt, E. V. & Ferreira, D. (2000). Polyphenols, condensed tannins, and other natural products in Onobrychis viciifolia (sainfoin). Journal of Agricultural and Food Chemistry 48, 3440–3447.Google Scholar
McNabb, W. C., Waghorn, G. C., Barry, T. N. & Shelton, I. D. (1993). The effect of condensed tannins in Lotus pedunculatus on the digestion and metabolism of methionine, cystine and inorganic sulphur in sheep. British Journal of Nutrition 70, 647–661.Google Scholar
McSweeney, C. S., Palmer, B., McNeill, D. M. & Krause, D. O. (2001). Microbial interactions with tannins: nutritional consequences for ruminants. Animal Feed Science and Technology 91, 83–93.Google Scholar
Min, B. R., Barry, T. N., Attwood, G. T. & 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.Google Scholar
Molan, A. L., Attwood, G. T., Min, B. R. & McNabb, W. C. (2001). The effect of condensed tannins from Lotus pedunculatus and Lotus corniculatus on the growth of proteolytic rumen bacteria in vitro and their possible mode of action. Canadian Journal of Microbiology 47, 626–633.Google Scholar
Mueller-Harvey, I. (2006). Unravelling the conundrum of tannins in animal nutrition and health. Journal of the Science of Food and Agriculture 86, 2010–2037.Google Scholar
Novobilský, A., Mueller-Harvey, I. & Thamsborg, S. M. (2011). Condensed tannins act against cattle nematodes. Veterinary Parasitology 182, 213–220.Google Scholar
Patra, A. K. & Saxena, J. (2011). Exploitation of dietary tannins to improve rumen metabolism and ruminant nutrition. Journal of the Science of Food and Agriculture 91, 24–37.Google Scholar
Pellikaan, W. F., Hendriks, W. H., Uwimana, G., Bongers, L. J. G. M., Becker, P. M. & Cone, J. W. (2011 a). A novel method to determine simultaneously methane production during in vitro gas production using fully automated equipment. Animal Feed Science and Technology 168, 196–205.CrossRefGoogle Scholar
Pellikaan, W. F., Stringano, E., Leenaars, J., Bongers, D. J. G. M., Van Laar-Van Schuppen, S., Plant, J. & Mueller-Harvey, I. (2011 b). Evaluating effects of tannins on extent and rate of in vitro gas and CH4 production using an automated pressure evaluation system (APES). Animal Feed Science and Technology 166–167, 377–390.Google Scholar
Regos, I., Urbanella, A. & Treutter, D. (2009). Identification and quantification of phenolic compounds from the forage legume sainfoin (Onobrychis viciifolia). Journal of Agricultural and Food Chemistry 57, 5843–5852.Google Scholar
Ramírez-Restrepo, C. A. & Barry, T. N. (2005). Alternative temperate forages containing secondary compounds for improving sustainable productivity in grazing ruminants. Animal Feed Science and Technology 120, 179–201.Google Scholar
Sas (Statistical Analysis System) (2002). Sas/Stat Software, Version 9.1. Cary, NC, USA: SAS Institute Inc.Google Scholar
Silanikove, N., Perevolotsky, A. & Provenza, F. D. (2001). Use of tannin-binding chemicals to assay for tannins and their negative postingestive effects in ruminants. Animal Feed Science and Technology 91, 69–81.Google Scholar
Singh, B. & Bhat, T. K. (2001). Tannins revisited-changing perceptions of their effects on animal system. Animal Nutrition and Feed Technology 1, 3–18.Google Scholar
Tavendale, M. H., Meagher, L. P., Pacheco, D., Walker, N., Attwood, G. T. & Sivakumaran, S. (2005). Methane production from in vitro rumen incubations with Lotus pedunculatus and Medicago sativa, and effects of extractable condensed tannin fractions on methanogenesis. Animal Feed Science and Technology 123–124, 403–419.CrossRefGoogle Scholar
Van Kessel, J. A. S. & Russell, J. B. (1996). The effect of pH on ruminal methanogenesis. FEMS Microbiology Ecology 20, 205–210.Google Scholar
Van Soest, P. J. (1994). Nutritional Ecology of the Ruminant. Ithaca, NY, USA: Cornell University Press.Google Scholar
Van Soest, P. J., Robertson, J. B. & Lewis, B. A. (1991). Methods for dietary fiber, neutral detergent fiber, and nonstarch polysaccharides in relation to animal nutrition. Journal of Dairy Science 74, 3583–3597.Google Scholar
Waghorn, G. C. (1990). Effect of condensed tannin on protein digestion and nutritive value of fresh herbage. Proceedings of the Australian Society of Animal Production 18, 412–415.Google Scholar
Waghorn, G. C. (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.Google Scholar
Waghorn, G. C. & Shelton, I. D. (1997). Effect of condensed tannins in Lotus corniculatus on the nutritive value of pasture for sheep. Journal of Agricultural Science, Cambridge 128, 365–372.Google Scholar
Waghorn, G. C., Shelton, I. D. & McNabb, W. C. (1994). Effects of condensed tannins in Lotus pedunculatus on its nutritive value for sheep. 1. Non-nitrogenous aspects. Journal of Agricultural Science, Cambridge 123, 99–107.Google Scholar
Wang, Y., Douglas, G. B., Waghorn, G. C., Barry, T. N., Foote, A. G. & Purchas, R. V. (1996). Effect of condensed tannins upon the performance of lambs grazing Lotus corniculatus and lucerne (Medicago sativa). Journal of Agricultural Science, Cambridge 126, 87–98.Google Scholar
Williams, B. A., Bosch, M. W., Boer, H., Verstegen, M. W. A. & Tamminga, S. (2005). An in vitro batch culture method to assess potential fermentability of feed ingredients for monogastric diets. Animal Feed Science and Technology 123–124, 445–462.Google Scholar
Williams, A. R., Fryganas, C., Ramsay, A., Mueller-Harvey, I. & Thamsborg, S. M. (2014). Direct anthelmintic effects of condensed tannins from diverse plant sources against Ascaris suum . PloS ONE 9, e97053. DOI: 10.1371/journal.pone.0097053 Google Scholar