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Review

Received: 19 November 2009 Revised: 9 June 2010 Accepted: 2 August 2010 Published online in Wiley Online Library: 2 September 2010

(wileyonlinelibrary.com) DOI 10.1002/jsfa.4152

Exploitation of dietary tannins to improve rumen metabolism and ruminant nutrition


Amlan K Patraa and Jyotisna Saxenab
Abstract
Tannins (hydrolysable and condensed tannin) are polyphenolic polymers of relatively high molecular weight with the capacity to form complexes mainly with proteins due to the presence of a large number of phenolic hydroxyl groups. They are widely distributed in nutritionally important forage trees, shrubs and legumes, cereals and grains, which are considered as antinutritional compounds due to their adverse effects on intake and animal performance. However, tannins have been recognised to modulate rumen fermentation favourably such as reducing protein degradation in the rumen, prevention of bloat, inhibition of methanogenesis and increasing conjugated linoleic acid concentrations in ruminant-derived foods. The inclusion of tannins in diets has been shown to improve body weight and wool growth, milk yields and reproductive performance. However, the benecial effects on rumen modulation and animal performance have not been consistently observed. This review discusses the effects of tannins on nitrogen metabolism in the rumen and intestine, and microbial populations (bacteria, protozoa, fungi and archaea), metabolism of tannins, microbial tolerance mechanisms to tannins, inhibition of methanogenesis, ruminal biohydrogenation processes and performance of animals. The discrepancies of responses of tannins among different studies are attributed to the different chemical structures (degree of polymerisation, procyanidins to propdelphinidins, stereochemistry and CC bonding) and concentrations of tannins, and type of diets. An establishment of structureactivity relationship would be required to explain differences among studies and obtain consistent benecial tannin effects. c 2010 Society of Chemical Industry Keywords: bloat; conjugated linoleic acids; methanogenesis; nitrogen metabolism; ruminants; tannins

INTRODUCTION
The manipulation of the rumen microbial ecosystem to increase the efciency of rumen metabolism and ultimately the productivity of animals has long been a pertinent goal for nutritionists and rumen microbiologists. A number of chemical feed additives such as antibiotics, ionophores, methane inhibitors and defaunating agents have been introduced into ruminant nutrition to promote growth, improve feed utilisation and decrease methane production. However, concerns over the presence of chemical residues in animal products and the development of bacterial resistance to antibiotics1 have stimulated the search for safer natural alternatives that would be useful in organic livestock farming. Plants or plant extracts containing essential oils, tannins, saponins, avonoids and many other plant secondary metabolites have been shown to improve rumen metabolism, such as decreased methanogenesis and protein degradation in the rumen, increased microbial protein production and protein ow to the duodenum targeting specic groups of rumen microbial populations.2 8 Tannins were primarily considered as anti-nutritional biochemicals due to their adverse effects on feed intake and nutrient utilisation.9 Nevertheless, in recent years, they have been recognised as useful phytochemicals for modulating rumen microbial fermentation benecially. A number of reviews on responses of tannins to ruminants have been published which focused mainly on adverse effects of tannins on animal systems with some discussion on the positive effects on protein metabolism and prevention of bloat.3,6,9 14 The recent reviews by Mueller-Harvey3 and Waghorn6 discussed little on methane inhibition by tannincontaining forages. Since the latest reviews, a great number of

studies have been published on the effects of tannins on inhibition of methanogenesis and enrichment of conjugated linoleic acids (CLAs) in meat and milk from ruminants, which justify a fresh appraisal of the present scenario on the inuences of tannins on rumen metabolism and animal performance. This review discusses the effects of tannins on ruminal metabolism particularly highlighting the benecial effects such as N metabolism, prevention of bloat, inhibition of methanogenesis and ruminal biohydrogenation process to enrich CLAs in ruminant-derived products.

CHEMISTRY AND OCCURRENCE OF TANNINS


Tannins are water-soluble polyphenolic polymers of relatively high molecular weight and have capacity to form complexes mainly with proteins, to a lesser extent with carbohydrates due to the presence of a large number of phenolic hydroxyl groups. Tannins are usually divided into two groups: hydrolysable tannins (HTs) and condensed tannins (CTs). The HTs are complex molecules with a polyol as a central core, such as glucose, glucitol, quinic acids, quercitol and shikimic

Correspondence to: Amlan K Patra, Department of Animal Nutrition, West Bengal University of Animal and Fishery, Sciences, 37, K. B. Sarani, Belgachia, Kolkata 700037, India. E-mail: patra amlan@yahoo.com

a Department of Animal Nutrition, West Bengal University of Animal and Fishery Sciences, 37, K. B. Sarani, Belgachia, Kolkata, 700037, India b Coskata, 4575 Weaver Parkway, Warrenville, IL 60555, USA

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epigallocatechin subunits (64%), i.e. a prodelphinidin-type CT with an average molecular weight of 2200.26 It has been noted that low molecular weight CT oligomers are more reactive and have higher protein-precipitating capacities than high molecular weight polymeric tannins.27 The presence of prodelphinidins and procyanidins in different proportions in forages can also determine different biological efcacy. For example, prodelphinidins were more effective against abomasal nematodes than procyanidins.28 The direct evidence of structureactivity relationships on rumen metabolism has perhaps not been demonstrated. In general, it has been assumed that the benecial effects of CTs of L. corniculatus forage on animal performance and nitrogen metabolism are attributed to the predominance of procyanidins compared with the effects of CTs of L. pedunculatus.6

Figure 1. Monomeric units of condensed (catechin and gallocatechin) and hydrolysable tannins (gallic and ellagic acid).

EFFECTS OF TANNINS ON NITROGEN METABOLISM


Nitrogen metabolism in the rumen The quantity of protein owing from the rumen is a major factor determining the productivity of ruminant livestock. The protein reaching the abomasum consists of a mixture of dietary and microbial protein. Increased ow of protein from rumen depends on decreased proteolysis by rumen microorganisms and increased efciency of microbial protein synthesis. When ruminants are fed on high-quality fresh forages containing a high concentration of N [2535 g kg1 dry matter (DM)] most of the proteins become rapidly soluble during mastication, releasing 5665% of the protein concentration in the rumen as soluble protein. Consequently, a large amount of soluble protein is degraded by rumen microorganisms resulting in surplus levels of ammonia (2035%) which is absorbed from the rumen and excreted in urine.29 Therefore, a reduction of protein degradation in the rumen will increase the quantity of protein digested in the small intestine. It is generally agreed that tannins decrease the rate of protein degradation in the rumen (Fig. 2). Condensed tannins in L. pedunculatus and L. corniculatus forages slowed down the rates of both solubilisation and degradation of forage protein to ammonia.30 32 Al-Dobaib33 reported that the rate of degradation and effective degradability of protein of lucerne hay were decreased by addition of quebracho tannins (2030 g kg1 DM). The decreased rate and extent of protein degradation in the rumen as observed due to feeding of tannin-rich feeds could lower ammonia concentrations in the rumen34 and hence urea N excretion in urine,34 38 which is advantageous environmentally. Puchala et al.39 also reported that ruminal ammonia N concentrations (3.7 and 9.9 mg dL1 ) were lower in goats fed CT-containing pasture Sericea lespedeza than crabgrass/tall fescue that might have been due to reduced protein breakdown in the rumen. The microbial protein outow from the rumen estimated by the excretion of urinary purines in sheep fed on a diet of dried leucaena hybrid KX2 (116 g CT kg1 DM) was not changed.40 Min et al.14 reported that CTs progressively increased the duodenal non-ammonia N, whereas rumen microbial protein outow was little affected. There are some studies that reported an improvement of microbial protein synthesis. Tamarind (Tamarindus indica) seed husk (140 g tannins kg1 DM) improved the efciency of microbial protein synthesis in vitro.41 Quebracho tannins also increased microbial protein synthesis in a lucerne diet fed to sheep at dosages of 10 and 20 g kg1 of DM, but not at 30 g kg1 of DM.33 Komolong et al.42 did not observe any

acid, which is partially or totally esteried with a phenolic group, i.e. gallic acid (3,4,5-trihydroxy benzoic acid; gallotannins) or gallic acid dimer hexahydroxydiphenic acid (ellagitannins)15 (Fig. 1). The resultant phenolic groups may further be esteried or oxidatively cross-linked to yield more complex HTs.15 Hydrolysable tannins are susceptible to hydrolysis by acids, bases or esterases yielding polyol and the constituent phenolic acids.15 The CTs, or proanthocyanidins, are mainly polymers of the avan-3-ol (epi)catechin and (epi)gallocatechin units, which are linked by C4C8 and C4C6 interavonoid linkages.16,17 Many other monomers of CTs, e.g. prosetinidins, probinetidins and proguibortinidins, are also present.15 Quebracho tannins are largely prosetinidins.18 In procyanidins and prodelphinidins, C4C8 and C4C6 linkages with a ratio of about 3 : 1 are more common and the majority of tannins in these classes are of mixed stereochemistry with 2,3-cis to 2,3-trans ratios between 9 : 1 and 5:5.19 The number of monomeric units can vary and this determines the degree of polymerisation from di-, tri- and tetraavonoids to higher oligomers. These can then produce an innite variety of chemical structures, which in turn could produce different biological properties.6 The CTs are degraded to form monomeric anthocyanidins (e.g. cyanidins and delphinidins) pigments upon treatment with acid butanol reaction.15,20 The CTs can react by hydrogen bonding with plant protein to form stable and insoluble CTprotein complexes at pH 3.57.0, which dissociate and release protein at pH <3.5.21 Tannins are widely distributed in nutritionally important forage trees, shrubs and legumes, cereals and grains that often limit their utilisation as feedstuffs. Generally, tannin concentrations are greater in vulnerable parts of the plants, i.e. new leaves and owers,22 24 and various factors such as temperature, light intensities, water and nutrient stress, soil quality and topography inuences the concentrations of tannins in plants.23,24 Both HTs and CTs may occur in the same plant, but some plants may contain predominantly HTs whereas others contain CTs.15 Again, although CTs in plants represent a mixture of different monomeric units, a particular type of CT may be predominant in a particular plant, which may explain different physiological effects and animal performance.6 For instance, the CT from Lotus corniculatus (birdsfoot trefoil) predominantly has catechin subunits (67%), i.e. a procyanidin-type CT with an average molecular weight of 1900,25 whereas the CT from Lotus pedunculatus (big trefoil) has

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AK Patra, J Saxena

Figure 2. Schematic representation of the effects of tannins on ruminal metabolism and ruminant performance. MFN, metabolic faecal nitrogen; CLA, conjugated linoleic acids; PUFA, polyunsaturated fatty acids; VFA, volatile fatty acids; GI, gastrointestinal.

Figure 3. Factors that may affect formation and dissociation of a tanninprotein complex and antibacterial activities of tannins in the gastrointestinal tract.

improvement on protein metabolism such as protein degradation and post-ruminal protein supply in sheep fed lucerne forage and low to moderate levels (060 g kg1 DM) of quebracho tannins as liquid drench, which was not clear although the study was of short duration (17 days). Nevertheless, it appears that tannins in diets may be predominantly advantageous by reducing degradation of protein in the rumen (Fig. 3) and in some cases improving microbial protein synthesis. This increases total supply of non-ammonia N to the duodenum and absorption from intestine.43 45 The reduction of protein degradation in the rumen may occur due to the formation of tanninprotein complexes in the rumen pH and inhibition of the growth and activities of proteolytic bacterial populations. Both CTs and HTs interact with proteins by forming hydrogen bonds between the phenolic groups of tannins and carboxyl groups of aliphatic and aromatic side chains of proteins and through hydrophobic interaction.3 The binding strength

of the tanninprotein interactions determines the responses of tannins on protein digestibility in the digestive tract.3 Besides the formation of tanninprotein complexes, reduction in proteolysis might be attributed to direct effects of CTs on microbial proteolytic enzyme activity or to indirect effects on rumen metabolite concentration that can regulate proteolytic activity in some bacteria.46,47 Condensed tannins have been shown to inhibit endogenous enzyme activity.48,49 It is suggested that at higher tannin/protein ratios, the inhibition of proteolysis is likely due to polyphenolic compounds covering the protein surface50 leading to interference with the interaction of enzyme and substrate. The in vitro studies suggested that the minimal concentration of a CT (g g1 of protein) needed to reduce proteolysis is 1 : 10 (w/w)51 or 1 : 12 (w/w).21 The effects of CTs on plant protein degradation and rumen microbes depend upon the chemical structure and molecular weight

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Dietary tannins to improve rumen metabolism and ruminant nutrition of tannins (Fig. 3).25,26,52 Gallic acid, which is a precursor of gallotannins, did not affect in vitro protein degradation of alfalfa protein, whereas tannic acid and quebracho tannins showed strong protein protection from ruminal degradation, indicating the similarity in biological effect of both HTs and CTs.53 Monomers have no protein-precipitating properties, while dimers, trimers, tetramers and other oligomers are capable of precipitating protein.19 Molan et al.54 showed that the effectiveness of decreasing the rate of proteolysis of soluble leaf protein extracted from white clover by mixed rumen microbes in vitro was more for trimers than dimers, and pentamers were more effective than dimers, trimers and tetramers procyanidins extracted from apple skin. Maximum protein-binding ability of CTs occurs with a molecular weight range of 5002000,19 whereas an increased degree of polymerisation (i.e. molecular weight) could be associated with less protein binding ability.17 At similar concentrations of CTs (0.251.75 mg mg1 of total soluble protein), CT of L. pedunculatus was more effective than L. corniculatus in protecting plant protein from degradation.11 The source of CTs, probably depending upon the types of monomers of CTs, may affect the ruminal degradation of protein. The CTs from Calliandra calothyrsus and Flemingia macrophylla had more effect on the degradation of soybean protein than CT from L. leucocephala.55 Condensed tannins with high amounts of prodelphinidins have greater protein-precipitating properties.10,56 Therefore, it appears that there are interactions between prodelphinidin content and molecular weight of tannins for protein precipitation with lower molecular weight and greater prodelphinidin content having higher protein-precipitating ability. Proteins also differ greatly in their afnity for phenolics. Proteins that have a high molecular weight, together with an open and exible tertiary structure bind strongly with phenolics.57 The CTprotein complex is not dissociated by rumen microbes,58 whereas the HTprotein complex is degraded as a result of depolymerisation of tannin polymers by cleaving the ester linkages between glucose and the phenolic subunits by the enzymes (tannin acylhydrolases and esterases) secreted by the rumen microbes.13,59 The tanninprotein complex is dissociated in the abomasum at pH <3.5 and in the intestine at pH >7 and protein is available for digestion in the small intestine.3,12,21,60 However, tannins differ in their ability to bind protein at rumen pH and thus reversibility of the process post-ruminally may also differ. Nitrogen metabolism in the abomasums and intestine The absorption process depends upon the reversibility of the proteintannin complex post-ruminally as tannins differ in their ability to bind protein at rumen pH.61 Occasionally, the tanninprotein complexes may not be dissociated fully depending upon the post-ruminal pH and tanninprotein complex formed, which again could be attributed to differences in the structures of tannins and proteins.3 Tannins in L. pedunculatus and in Desmodium ovalifolium protected protein in the rumen and dissociated from the complexed protein in the abomasum and intestines.44,60 However, the inclusion of quebracho CT (10 and 20 g kg1 of DM) in diets of cattle62 and feeding of O. viciifolia forage,36 C. calothyrsus and F. macrophylla legume shrubs37 to sheep reduced apparent protein digestibility. The greater faecal N excretion has been shown in many studies with tannin-containing diets12,38,42,63,64 where probably tanninprotein complexes were not completely dissociated in the abomasums and lower digestive tract. The L. lecucocephala CTprotein complexes were more resistant in the abomasal conditions than the complexes formed with C. calothyrsus and F. macrophylla.55 Tannins may also interact

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with digestive enzymes65 and the epithelium lining the digestive tracts66 if signicant amount of tannins reach the duodenum, and therefore reduce amino acid absorption from the intestine.67 Komolong et al.42 reported that increasing concentrations of quebracho CT in the lucerne-based diet in sheep linearly increased non-ammonia nitrogen ow at the terminal ileum while there was no change in the non-ammonia N ow to abomasums or ammonia concentrations in the rumen. This study clearly demonstrated that quebracho tannins lowered the apparent digestibility and absorption of amino acids at the small intestine. Besides, dietary tannins have been implicated to increase metabolic faecal nitrogen excretion,68 which may also account for a reduction of apparent protein digestion. All these factors might increase the faecal N output on tannin-based diets. The tannins shift in the site of N metabolism from rumen to the lower digestive tract and large intestine. Therefore, inuences of tannins on N metabolism in the large intestine could be important. The N in these parts of the digestive tract represents undigested feed N, undigested bacterial N, indigestible feed N and endogenous N secreted or sloughed from earlier sections. There is no information available regarding the effects of tannins on N metabolism in the caecum and large intestine. In sheep, about 0.52 g of N daily can disappear from the large intestine,69 which may correspond to about a third of the apparently digestible N of feeds. Although most of the N is absorbed as ammonia, some of it will be returned to the rumen for a further contribution to N metabolism.69 The pH of the large intestine could be 5.57.0, where free tannins, if not degraded, may again bind with the proteins and thus decrease recycling of N. This may be another reason in contributing increased faecal N and exacerbating N utilisation when tannins are added in the diets. Nevertheless, shifting excretion pattern of nitrogen from urine to faeces and formation of CTprotein complex are benecial environmentally. First, faecal nitrogen is mainly in the organic form, which is less volatile, whereas urinary nitrogen is largely in the form of urea, which is more rapidly hydrolysed to ammonia and nitried to nitrate.70,71 The nitrate could leach into groundwater causing water pollution, and is also converted to nitrous oxide (a greenhouse gas) accounting for about 65% of global anthropogenic nitrous oxide emissions.72 Secondly, a CTprotein complex in faeces dissociates slowly in the soil because mineralisation of the complex is inhibited, and the faeces decompose more slowly compared with faeces without CT.71,73 Therefore, decreased nitrogen excretion in the urine could reduce ammonia and nitrous oxide emissions into the atmosphere.70,74

EFFECTS OF TANNINS ON CARBOHYDRATE DIGESTION


The apparent digestion of soluble carbohydrates appears to be unaffected by tannins. High concentrations of CTs in L. pedunculatus (95 and 10.6 g kg1 of DM) reduced rumen digestion of readily fermentable carbohydrate and hemicellulose, but this was counteracted by increased post-ruminal digestion.43,44 Carbohydrate digestion in sheep fed on L. corniculatus containing 2535 g CT kg1 (DM basis) was not affected by CT.45 Inclusion of quebracho tannins (containing 750 g CT kg1 ) at a dosage of 22.5 g kg1 to lucerne hay decreased the bre digestibility; whereas no effect was noted at dosages of 7.5 and 15 g CT kg1 of DM.33 The potential extent of digestion up to 0.47 mg mL1 was unaffected for any tannin. In a study of sheep, Tiemann et al.37 reported that replacement of a Vigna unguiculata legume (tannin-free) with

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www.soci.org C. calothyrsus and F. macrophylla depressed the organic matter and bre digestibility. Tannins present in Terminalia chebula also decreased DM degradability at high concentration in vitro.75 However, when T. chebuala was fed to sheep at 10 g kg1 of total DM intake, the digestibility of nutrients and bre fractions increased,76 which could be attributed to the increased numbers of brolytic bacterial populations in the rumen.77 Higher concentrations of tannins in diets, which remain free after binding with proteins, may depress bre digestion by complexing with lignocellulose thus preventing microbial digestion78 or by directly inhibiting cellulolytic microorganisms7 and activities of brolytic enzymes79 or both. Although the nature of binding with carbohydrates has not been determined it is stated that this binding is relatively independent of pH and is inuenced by the type of tannins (molecular weight, exibility and water solubility) included in the diets.19 Makkar et al.80 studied different sources and dosages of tannins on the rate of fermentation of hay in an in vitro study. The decrease in rate of fermentation of DM was 3% and 17% for Q. incana, 6% and 21% for D. cinerea and 7% and 27% for A. barteri at 0.47 and 0.93 mg mL1 tannins in the medium, respectively. It indicates that different tannins exhibit different effects on DM digestibility at the same inclusion level. Tannins and saponins interaction was found to be additive.80 The presence of Calliandra tannins in the diet (2030 g tannin kg1 DM) reduced the populations of bre-degrading bacteria, the efciency of microbial protein synthesis was not affected.81 McAllister et al.52 showed that CTs from different legume forages had a varied extent of inhibition of rumen brolytic bacteria, Fibrobacter succinogenes. Tannins with low molecular weight had greater inhibitory effects on rumen microbes. The reduced rate of carbohydrate digestion, especially bre, may decrease total volatile fatty acid concentrations in the rumen.62,75

AK Patra, J Saxena

EFFECTS OF TANNINS ON RUMINAL METHANOGENESIS


Methane produced during anaerobic fermentation in the rumen represents a feed energy loss and contributes to the greenhouse effect in the environment. Therefore, reducing methane emission has been an important objective for ensuring the sustainability of ruminant production. Methane is produced normally during fermentation of feeds by methanogenic archaea. The removal of protozoa can also reduce methane production as some population of methanogens remains attached with protozoa.82 Tannin-containing forages and tannin extracts have been demonstrated to decrease methane production both in vivo and in vitro (Table 1). Tannins present in C. calothyrsus and O. viciifolia reduced methane release per gram of organic matter degraded in Rusitec.82,92 Woodward et al.93 investigated the feeding of Hedysarum coronarium (sulla) on methane emissions and milk yield in Friesian and Jersey dairy cows. Cows grazing on H. coronarium had higher daily dry matter intake (13.1 vs. 10.7 kg DM) and daily milk solid production (1.07 vs. 0.81 kg) than grazing perennial ryegrass pasture. Total daily methane emission was similar (253.9 vs. 260 g). However, cows fed on H. coronarium produced less methane per kg DM intake (19.5 vs. 24.6 g) and per kg milk solid yield (243.3 vs. 327.8 g). Similar trends in methane emissions and milk production have been observed in sheep fed L. corniculatus and L. pedunculatus silage.94 There was also a 16% reduction in methane production in lambs fed on L. pedunculatus, which is ascribed due to the presence of CTs.95 Another CT-containing forage, S. lespedeza (177 g CT

kg1 of DM), decreased methane emission (7.4 vs. 10.6 g d1 and 6.9 vs. 16.2 g kg1 DM intake for S. lespedeza and crabgrass/tall fescue, respectively) in Angora goats.39 Dry matter intake (1.11 vs. 0.67 kg d1 ) and digestible DM intake (0.71 vs. 0.51 kg d1 ) were greater for S. lespedeza than for crabgrass/tall fescue in this study. Animut et al.64 also observed that feeding different levels of Kobe lespedeza decreased methane production linearly in goats and it has been attributed to the presence of CTs. Similarly, addition of CTs from Acacia mearnsii to forage-fed sheep83 and dairy cattle38 decreased methanogenesis substantially. Methane production was also inhibited by inclusion of a methanol extract of pericarp of T. chebula (a tropical fruit), in vitro, up to 90%.75 Ground materials of the pericarp of T. chebula also inhibited methane production in vitro88 and in sheep fed 10 g kg1 of DM intake.76 This is assumed to be due to presence of tannins, especially HTs, in this fruits. Hydrolysable tannin extracts,96 such as gallotannic acid inhibited 50% methane production (up to 700 mg L1 ) with lower toxicity associated with monomers versus polymers. Methane production was not affected in a number of studies with tannin-containing diets,62,91 probably due to low dosage of tannin addition. Tavendale et al.87 reported that methane production (mL g1 DM) at 12 h for M. sativa (25 mL) was higher than L. pedunculatus (17.6 mL) that contains 1.0 g CT kg1 and after addition of polyethelene glycol increased methane production for L. pedunculatus (17%) but not for M. sativa. They also studied the mechanism of inhibitory effects of extractable CT fractions from L. pedunculatus on the common rumen methanogens Methanobrevibacter ruminantium, strains YLM-1 and DSM1093. Oligomeric CT fractions were inactive against both strains, as determined by methane production measurements. The polymeric fraction completely inhibited methane production. Inhibitory effects in broth culture for strain YLM-1 were bacteriostatic, while strain DSM1093 did not recover growth, as indicated by methane production, even upon prolonged incubation. In a plate assay, the zone of inhibition with the polymeric fraction remained after a further week of incubation. In sheep, the inclusion of the tannin-rich browses C. calothyrsus and F. macrophylla reduced methane emissions per day and per unit of feed and energy intake by up to 24% relative to a tannin-free legume Vigna unguiculata supplemented diet but this have been mostly due to the result of reduced organic matter and bre digestion as bre digestion was also reduced in this study.37 Tannins have been shown to lower protozoal numbers,7 which may also decrease protozoal-associated methanogenesis.97 Overall, the inhibitory effects of tannins on rumen methanogenesis have been ascribed to direct effects on methanogenic archaea, protozoal-associated methane production and indirectly through a depression of bre digestion in the rumen.

EFFECTS OF TANNINS ON RUMINAL BIOHYDROGENATION


Increasing the concentrations of CLAs in foods derived from ruminants has been of interest recently in many research studies due to its benecial effects on health, such as anti-cancer properties, reduced risks for cardiovascular diseases, reduction of body fat accretion and modulation of the immune system. The CLAs represent cis and trans isomers of linoleic acid (C18 : 2) with conjugated double bonds, e.g. cis-9, trans-11 C18 : 2 (also called rumenic acid and a predominant isomer in meat and milk) and trans-10, cis-12 C18 : 2 (Fig. 4).98 The CLA concentrations in ruminant-derived foods can be increased by nutritional and

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Table 1. Effects of tannins on methane production and related digestibility, rumen fermentation and protozoal numbers Tannin source Acacia mearnsii extract (CT 725 g kg1 ) Castanea sativa wood extract (HT 200 g kg1 ) C. sativa wood Experiment Sheep Rusitec Sheep Dosage 41 g kg1 diets 0.5 and 2.5 g kg1 DM of effective tannins 5 and 10.1 g kg1 DM equivalent to 1 and 2 g kg1 pure tannins 0.5 mL per 30 mL (0.2 g substrate) Experimental group grazed on L. cuneata pasture Lespedeza: sorghumsudan grass (1 : 2, 2 : 1 and 3 : 0) L. striata as sole feed L. corniculatus forage 0.331 g L1 Diet Ryegrass, ryegrass : alfalfa (1 : 1) Grass silage and hay : barley (77 : 23) Hay : barley-based concentrate (1 : 1) Wheat straw : concentrate (1 : 1) Control group grazed on crabgrass/tall fescue Compared with sorghumsudan grass as control Compared with L. striata + polyethylene glycol Compared with Medicago sativa Wheat straw : concentrate (1 : 1) Wheat straw : concentrate (1 : 1) Wheat grass Wheat grass in vegetative stage Wheat grass in reproductive stage Barley silage 69.5%, barley grain 21.5% Wheat straw : concentrate (1 : 1) Wheat straw : concentrate (1 : 1) Wheat straw : concentrate (1 : 1) Wheat straw : concentrate (1 : 1) Effect DG, TVFA, TPZ, =; A/P, MT, DG, TVFA, A/P, TPZ, MT, = DG, TVFA, A/P, TPZ, =; MT, DG, TVFA, A/P, =; A/P, TPZ, MT, with ethanol extracts TVFA, A/P; =; MT, DG, TPZ, MT, ; TVFA, A/P, = DG, TPZ, MT, ; TVFA, A/P, = TVFA =; A/P, ; MT, TVFA, A/P, TPZ, =; MT, TVFA, ; A/P, ; DG, TPZ, =; MT, at the highest dosage MT, DG, MT, = DG, MT, DG, MT, =; TVFA, A/P DG, TVFA, A/P TPZ, =; MT, at the high dosage TVFA, A/P, =; DG, TPZ, MT, TVFA, A/P, TPZ, =; MT, DG, ; MT, Reference 83 84 85

Emblica ofcinalis seed pulp extracts Lespedeza cuneata (177 g CT kg1 ) Lespedeza striata forage

In vitro

75

Goats

39

Goats

64

L. striata forage Lotus corniculatus (99 g CT kg1 ) Populus deltoides leaves

Goats Glass bottle In vitro

86 87 88

P. deltoides leaves extracts

In vitro

0.5 mL per 30 mL (0.2 g substrate) 12 g L1 10 and 20 g kg1 of DM intake 10 and 20 g kg1 of DM intake 10 and 20 g kg1 of DM intake 0.5 mL per 30 mL (0.2 g substrate) 0.5 mL per 30 mL (0.2 g substrate) 0.331 g L1 10 g kg1 DM intake

89

Quebracho tannins (750 g CT kg1 ) Quebracho tannins (750 g CT kg1 ) Quebracho tannins (750 g CT kg1 ) Quebracho tannins (910 g CT kg1 ) Terminalia belerica seed pulp extracts Terminalia chebula pulp extracts T. chebula seed pulp

In vitro In vitro In vitro Beef cattle In vitro

90 91 91 62 75

In vitro

75

In vitro

77

T. chebula seed pulp

Sheep

76

DG, digestibility; TPZ, total protozoal numbers; MT, methane production; TVFA, total volatile fatty acid concentration; CT, condensed tannins; HT, hydrolysable tannins; DM, dry matter; A/P, acetate to propionate ratio; =, unaffected; , decreased; , increased. Dose levels have been expressed as g L1 of medium or g kg1 substrate (additives have not been considered as substrates here). Ethanol and methanol extracts.

management practices that facilitate higher forestomach output of CLAs and vaccenic acid (trans-11 C18 : 1) for absorption and incorporated into animal tissues.98 Many ruminal bacteria species of the genera Butyrivibrio, Ruminococcus, Treponema-Borrelia, Micrococcus, Megasphaera, Eubacterium, Fusocillus and Clostridium are known to be associated in ruminal biohydrogenation.99 101 Butyrivibrio spp. are most active species among the group A bacteria, which form CLA from linoleic acid, while few species of bacteria such as Fusocillus spp. and Clostridium proteoclasticum (group B) convert vaccenic acid to stearic acid.100 102 Therefore, it has been suggested that selective inhibition of group B bacteria

without affecting group A bacteria may provide more vaccenic acids and CLAs.99,100 The ability of plant extracts including tannins to modify the fatty acid composition of ruminant-derived food products (i.e. milk or meat) has received great attention recently. There is very limited information pertaining to the effects of tannins on ruminal biohydrogenation process and CLA content in meat and milk. The CTs have been shown to inhibit the growth of many ruminal bacteria7,103,104 including bacteria associated with ruminal biohydrogenation. Durmic et al.101 screened several plants for their ability to modify ruminal biohydrogenation process. In this

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Figure 4. Biohydrogenation process in the rumen and tissues (modied from Harfoot and Hazlewood99 and Bauman et al.98 ). Specic inhibition of group B bacteria by tannins may increase concentrations of polyunsaturated fatty acids and conjugated linoleic acid in tissues.

study, extracts of 37 plants inhibited the growth of C. proteoclasticum, of which 10 did not affect the growth of B. brosolvens. The active components of these plants have not been elucidated. Sivakumaran et al.105 demonstrated that all three fractions (i.e. low, medium and high molecular weight) of proanthocyanidins from Dorycnium rectum forage inhibited the growth of C. proteoclasticum at concentrations of 100, 200 and 300 mg L1 of in vitro medium, whereas although low and medium molecular weight fractions inhibited the growth of Butyrivibrio brisolvens at these concentrations, the high molecular weight fraction stimulated the growth of this bacterium at the concentration of 100 mg L1 . More recently, Vasta et al.106 demonstrated that inclusion of quebracho tannin (9.6% of DM intake) to a barley-based concentrate and lucerne hay diet for sheep increased the population of B. brisolvens (8.76 vs. 4.22% of total bacteria), while the growth of C. proteoclasticum (2.77 vs. 3.99% of total bacteria) reduced. The total number of bacteria was not affected in their study. This selective activity of tannins to rumen bacteria could be benecial nutritionally by altering the ruminal biohydogenation process and hence enhancing CLA content of ruminant-derived products. Khiaosa-Ard et al.107 reported that addition of CT (78.9 g kg1 of DM) inhibited the last step of C18 : 3 biohydrogenation in Rusitec. This inhibition led to the accumulation of trans-11 C18 : 1 in the feed residues but had no effect on the losses of C18 : 3 compared with the control treatment. Vasta et al.108 also reported that the concentration of trans-11 C18 : 1 increased while concentration of total CLA did not increase in in vitro ruminal uid. In in vivo studies, addition of quebracho tannins in the diet of sheep resulted in an increased concentrations of trans-11 C18 : 1 in the rumen106,109 and cis-9, trans-11 C18 : 2 and poly unsaturated fatty acids in lamb meat.109 In another study, quebracho tannins (89.3 g kg1 of DM) increased the concentrations of C18 : 2n-6 and polyunsaturated fatty acids in lamb meat.110 Kronberg et al.111 reported that quebracho CT (200 g kg1 of axseed) reduced biohydrogenation of C18 : 3 in axseed (13 vs. 43%) in an in vitro batch culture. However, feeding tannin-treated axseed to beef cattle in the same study did not increase the concentrations of C18 : 3 and 18 : 5 in plasma neutral lipids.111 Benchaar and Chouinard112 also did not observe any changes in milk fatty acid composition by feeding a quebracho tannin extract (150 g day1 , i.e. 4.5 g kg1 of DM; 700 g tannins kg1 of DM) to dairy cows. These discrepancies among the in vivo studies could involve dosage and type of CT, type of diets and resistance of ruminal microorganisms to tannins. A recent study has demonstrated that the trans-11 C18 : 1 concentration in intramuscular fatty tissue was increased by feeding of quebracho CT to lambs in a concentrate-based diet (1.14 vs. 0.45 mg g1 fresh tissue),

while this concentration was not affected by CT in the fresh vetch herbage-based diet.110 Besides, tannins may indirectly regulate the 9 -desaturase enzyme expression in tissues via modulation of fatty acids absorption from the rumen resulting in changes of fatty acids composition in tissues,110 which indicates that ruminal concentrations of CLA may not be reected in the tissues.

EFFECTS OF TANNINS ON BLOAT PREVENTION


Bloat occurs when the rate of gas production exceeds the rate of gas expelled by normal eructation or the eructation mechanism is inhibited or impaired resulting in an accumulation of gas in the rumen. Free-gas or feed-lot bloat occurs sporadically in feed-lot cattle, but frothy bloat is more common in ruminants grazing legume forages113 or immature wheat pasture.90 The formation of stable foam in the rumen of feed-lot cattle can result in the cardia being covered by foam, which inhibits eructation of gas.113 Frothy bloat is associated with increased production of gas and slime resulting from changes in the microbial populations combined with presence of soluble protein in ruminal uid coming from legume forages.90,114 Tannins have the ability to precipitate soluble protein fractions which have been implicated in the reduction of bloat grazing CTcontaining legume forages.12,115,116 The substitution of a portion of lucerne or mixed cropping with CT-containing forages (e.g O. viciifolia) may prevent incidences of bloat.24,116 Li et al.117 mentioned that a minimum concentration of 50 g CT kg1 in forages is needed to consider forages bloat-safe. Therefore, plant breeding and genetic engineering technologies have been employed to increase the CT concentrations in some legume forages.118 Besides feeding tannin-containing forages, tannin extract can be fed to animals to prevent bloat problems. Min et al.91 reported that feeding a CT extract reduced the occurrence of bloat in steers grazing wheat pasture. Ruminal uid supplemented with CTs and incubated with fresh wheat forage decreased the rate of gas production in vitro.90,91 A decrease in severity of bloat due to feeding CTs has been attributed to reduction of microbial activities, biolm production, and ruminal gas production.119

EFFECTS OF TANNINS ON RUMEN MICROBIAL POPULATIONS


The effects of tannins on rumen microbial populations have been discussed recently in detail.7 In brief, the effects of tannins on ruminal bacteria are reported to be dependent upon the species of microorganism and type or source of tannin.103,105

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Dietary tannins to improve rumen metabolism and ruminant nutrition Jones et al.103 studied the effects of CTs of the legume sainfoin (O. viciifolia) on growth and proteolysis by four strains of ruminal bacteria. They observed that growth of proteolytic bacteria (B. brisolvens, Ruminobacter amylophilus and Streptococcus bovis) was reduced by CT but had little effect on a strain of Prevotella ruminicola. Morphological changes occurred in the bacteria that were inhibited by tannins, whereas an extracellular material produced by P. ruminicola probably protected the bacteria from the direct action of tannins.103 Similarly, addition of phlorotannins at 0.5 g L1 to rumen cultures inhibited the growth of F. succinogenes, but had minimal effect on Ruminococcus avefaciens and R. albus, whereas the growth of S. ruminantium, S. bovis, R. amylophilus and Prevotella bryantii was stimulated.120 The antimicrobial activities of tannins are ascribed to the interactions of tannins with the extracellular enzymes secreted and the cell wall of bacteria causing morphological changes of the cell wall, tannin-induced membrane disruption, direct action on microbial metabolism, deprivation of substrates for microbial growth and chelation of cations by tannins reducing its availability to microbes.9,103,121,122 Chung et al.123 demonstrated that tannic acid inhibited the growth of some human intestinal bacteria, but not lactic acid bacteria. In their studies, addition of iron in the medium restored the growth of E. coli, which indicates that the iron-chelating properties of tannins contributed to the inhibitory activities. However, although methylgallate and propylgallate inhibited the growth of the intestinal bacteria, iron was not responsible for the growth inhibition.123 Muhammed et al.124 investigated the effects of tannic acid, ellagic acid, gallic acid and catechin on rumen fungus Neocallimastix frontalis strain RE1. All these compounds inhibited the cellulolysis and zoospore attachment to cellulose by this fungus. Gallic acid, ellagic acid and catechin showed more inhibitory effect to cellulolysis than tannic acid. However, ellagic acid was most inhibitory to zoospore attachment, perhaps indicating the involvement of different cell-surface receptors in this process. However, bredegrading ability of rumen fungi may be less sensitive to the inhibitory effects of CT compared to cellulolytic bacteria.125 The effects of tannins on rumen protozoa are variable. Salem et al.126 observed a linear increase in protozoal numbers in rumen uid of sheep fed on a lucernhay-based diets by addition of increased proportion of Acacia cyanophylla foliage, which contained 45 g CT kg1 of DM. Similarly, CT present in L. corniculatus and H. coronarium increased protozoal numbers in the rumen of sheep.22,127 There are many reports indicating inhibitory effect of tannins on rumen protozoa. Makkar et al.80 reported that quebracho CT (0.10. 4 mg mL1 media) signicantly reduced the numbers of total protozoa, entodiniomorphs and holotrichs, the effect being higher on holotrichs in Rusitec. Benchaar et al.128 did not observe any effect on protozoal numbers in dairy cattle fed quebracho tannins (CT concentrations of 700 g kg1 , 150 g day1 ) probably due to addition of a low dosage in the diet. The mechanisms of inhibition of rumen protozoa are not known.

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Figure 5. Tolerance mechanisms of bacteria to dietary tannins.

RESISTANCE OF RUMEN MICROORGANISMS TO TANNINS


Several species of tannin-tolerating bacteria have been identied, including Streptococcus gallolyticus, a strain related to Streptococcus bovis.122,129 Brooker et al.130 also isolated a tannin-resistant Streptococcus caprinus from feral goats browsing Acacia aneura (110140 g tannin kg1 DM). S. caprinus, which was absent in domestic goats and sheep and was able to grow in the medium

containing 2.5% (w/v) tannic acid. Trans-inoculation of these bacteria of rumen uid from feral goats to sheep fed on Acacia improved DM intake and nitrogen digestibility in sheep and the population was maintained for as long as the animal was fed the Acacia diet. An anaerobic diplococcoid bacterium, isolated from the rumen uid of goat fed on Desmodium ovalifolium (contains 170 g CT kg1 ), was able to grow in the presence of up to 30 g of tannic acid L1 of solution and this bacterium degraded tannic acid to pyrogallol.131 Similarly, Odenyo and Osuji132 isolated three strains of tannin-tolerant bacteria related to Selenomonas sp. from sheep, goat and antelope, which were able to grow in media containing 50 g L1 of tannin extract and 5070 g L1 of tannic acid. Several mechanisms have been proposed for the resistance mechanisms of the bacteria to tannins (Fig. 5). Some bacteria grown in the presence of tannin secrete exo-polysaccharides (glycoproteins) that form a protective layer around the cells and thus protect the cells from the action of tannins.133,134 Chiquette et al.135 demonstrated using transmission electron microscopy that ruminal bacteria produced a thick glycocalyx when grown in association with the high tannin containing L. corniculatus forage. Recently, Zoetendal et al.136 reported that Acacia mearnsii tannins up-regulated the cell envelop stress protein gene (suggested to be involved in outer membrane protein folding and cell envelope synthesis and tolerance mechanism towards to tannins) in Eschericha coli as determined by quantitative real-time polymerase chain reaction. Besides, the morphology of bacteria may be changed in the presence of tannins in media.133 Goel et al.137 also observed that Streptococcus species isolated from non-adaptive cattle were converted from diplococi to an elongated chain of 4050 cells with increasing concentrations of tannic acid in the media. Tolerance mechanism of bacteria to tannins may also involve degradation of tannins by bacteria. Tannin-degrading microorganisms have been isolated from several species of ruminants including sheep, goat, deer and elk that have access to tannin-rich forages.132 Some human intestinal bacteria such as Lactobacillus sp. and Bidobacterium sp. were inherently resistant to tannic acid because haem-containing enzymes are not present in these bacteria.123 Tannic acid has strong iron binding capability, which depletes iron from media for the growth of bacteria having haem-containing enzymes.123 Besides, bacteria grown in

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www.soci.org the presence of tannins may synthesise siderophores,121 which probably counteract the depletion of iron by tannins. In addition to the development of tolerance mechanisms by the rumen bacteria, animals themselves may develop tolerance to tannins by secreting increased amounts of proline-rich proteins in the saliva.138 These proteins have strong afnity for tannins and may be constitutive or inducible depending upon the species of the animals.3 The secretion of proline-rich proteins may diminish the responses of tannins to N metabolism.

AK Patra, J Saxena

METABOLISM OF TANNINS IN THE RUMEN


Rumen microbes are able to degrade simple plant phenolic compounds to some extent to counteract anti-nutritive effects of tannins. Phenolic glycosides such as rutin and naringin, and avonoid ring system of the common plant avonoids (e.g. quercitrin) are readily degraded in the rumen by hydrolysis of the glycoside and cleavage of the heterocyclic ring to acetate, butyrate, di- and monohydroxyphenolics, and phloroglucinol.139,140 The ester bonds and depside bonds of HTs are both cleaved in the rumen by Selenomonas ruminantium and Streptococcus spp. which produce esterase, tannin acylhydrolase59,129,137,141 to form gallic acid and ellagic acid. Gallic acid is then decarboxylated in the rumen to pyrogallol and converted to resorcinol and phloroglucinol before cleavage of the phloroglucinol ring to acetate and butyrate by rumen microorganisms.141,142 Sheep fed tannic acid and HTs from leaves of Terminalia oblongata (containing ellagitannins) excreted glucuronides of resorcinol and 2-carboxy-2 ,4 ,4,6-tetrahydroxy diphenyl 2,2 -lactone as urinary metabolites.142 Catechin and gallocatechin can be degraded to velerolactone and phenylpropionic acid by intestinal microorganisms, and glucuronic acid or sulphate conjugates of velerolactone have been observed to excrete through urine and faeces in rats and human.3,143 In contrast to HTs, the fate of CTs in the gastrointestinal tract is not clear. Some quantitative nutritional trials have shown apparent losses of 29.1% and 51.7% of CTs from Acacia barteri and Bauhania varigata, respectively, up to 24 h of fermentation in vitro with no further increase in the degradability of CT after 24 h.144,145 With radioactively labelled CTs, Perez-Maldonado and Norton146 detected substantial losses of 14 C-labelled CTs from Desmodium intortum in the gastrointestinal tract of sheep and goats. Wiryawan et al.147 noted that tannin-degrading bacteria isolated from goats exposed to tannins of Calliandra sp. were able to decrease tannic acid and CTs from the medium. Perez-Maldonado and Norton146 suggested that free CTs or breakdown products of CTs may be absorbed from the digestive tract. It has also been postulated that the apparent disappearance of CTs from the digestive tract can be a result of minor conformational changes in the reactive CT ring structure and consequently these polyphenols are not quantied by the analytical techniques.6,146,148 However, the cleavage of carboncarbon bonds of the avan-3-ol ring system (e.g. catechin and epicatechin) of CTs by ruminal microorganisms has not been conrmed, and these observations need to be validated by denitive experiments on microbial degradation of model CTs.13

EFFECTS OF TANNINS ON RUMINANT PERFORMANCE


The feed intake by animals is usually reduced for diets with high concentrations of tannins, which is suggested to be due to a reduction of palatability of diets, decreased rate of digestion in the

rumen and the development of conditioned aversion.3,6,24 Hervas et al.149 noted that the addition of quebracho tannins in the diet of sheep at 0, 0.5, 1.5 and 3 g kg1 BW (equal to 0, 28, 83 and 166 g kg1 DM) did not affect feed intake up to 1.5 g kg1 BW, but signicantly decreased at the highest dosage. Similarly, quebracho CTs up to 20 g kg1 of DM had no inuence on feed intake in cattle.62 It has generally been advised that tannin concentrations of greater than 50 g kg1 in diets may negatively affect feed intake whereas lower concentrations of tannins have no inuence on intake by ruminants.11,43,46,150 Further, diet and tannin interaction may inuence voluntary feed intake. For example, quebracho tannins (89.3 g kg1 of DM) reduced DM intakes in lamb fed fresh vetch (Vicia sativa) than the lambs fed the same herbage without tannins (768 vs. 956 g day1 ), whereas tannins did not affect the DM intakes in lambs fed a concentrate-based diet.110 The greater animal performance observed when diets contain moderate levels of tannins has generally been attributed to the protection of feed protein from degradation in the rumen, leading to an increase in the ux of essential amino acids to the small intestine and an increase in the absorption of essential amino acids to blood151,152 when tannins do not compromise intakes and digestion of feeds. Wang et al.153 reported that lambs grazing L. corniculatus had better wool growth and carcass gain than grazing lucerne, which was attributed to the presence of CTs (34 g kg1 ) in the diets. Inclusion of quebracho tannins at a dosage of 20 g kg1 (equivalent to 15 g CT kg1 ) to lucerne hay increased body weight gain and feed conversion efciency in lamb compared with control while dosages of 10 and 30 g kg1 had intermediate values.33 Similarly, L. corniculatus fed to lactating ewes increased milk yield, lactose and protein by 21, 12 and 14%, respectively, during mid and late lactation.154 Similar experiment with dairy cows were conducted by Woodward et al.155 and they reported that cows fed on L. corniculaus had 42% higher milk yields than those fed on L. corniculatus plus polyethylene glycol (to bind tannins), ryegrass and ryegrass plus polyethylene glycol, indicating that CTs in L. corniculatus resulted in increased milk yield. It was also responsible for a 57% increase in milk protein of cows fed on L. corniculatus. Lactating dairy cows fed diets containing 816% peanut skins (180 g CT kg1 ) resulted in higher DM intakes, milk yield and milk fat content but had lower milk protein content.34 Inclusion of 75 g tamarind seed husk, a tanninrich by-product (140 g CT kg1 ) per kg diet of cross-bred dairy cows also resulted in increased body weight gain and milk protein content in mid lactation.35 Ramirez-Restrepo et al.156,157 reported higher growth, reduced parasite burden, improved reproductive performance and wool production in lambs grazing L. corniculatus than perennial ryegrass (Lolium perenne)/white clover (Trifolium repens) pasture. One of the reasons for these effects could be possibly due to increased metabolisable protein supply, from the protein binding action of CT. Besides, the potential benecial biological effects of CTs in forages may also be mediated through the control of gastrointestinal parasites. Addition of CT (10 and 20 g kg1 of DM) in steers grazing winter wheat forages increased body weight gain.91 However, L. pedunculatus containing 7690 g CT kg1 of DM decreased rates of body weight gain and wool growth,158 which has been explained due to the presence of high concentrations or different types of CTs in forages.3,151 Recently, Grainger et al.38 reported that milk yield, fat and protein percentage of milk reduced when dairy cows were dosed daily with 163326 g CT from Acacia mearnsii. In this experiment, feed intake and digestibility were also decreased by A. mearnsii tannins. Beauchemin et al.62 did not note any signicant effect on growth

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Dietary tannins to improve rumen metabolism and ruminant nutrition and intakes when cattle were fed a forage-based diet (700 g kg1 ) supplemented with 10 and 20 g quebracho tannins kg1 of diet. In essence, the effects of tannins on ruminant productivity depend upon quality (e.g. degradability and composition of essential amino acids) and quantity of dietary protein, requirements of amino acids and status of other nutrients. Aerts et al.11 reviewed that forages containing moderate concentrations of CT (2040 g kg1 of DM) may exert benecial effects on protein metabolism; however, high dietary CT concentrations (60120 g kg1 of DM) may depress voluntary feed intakes, digestive efciency and animal productivity. However, the type of CT present in forages may greatly inuence voluntary feed intake and performance of animals. Diets containing as low as 26 g tannins kg1 from carob pulp (Ceratonia siliqua) resulted in a decrease of growth rate of lambs from 140 to less than 50 g per day159 whereas the CT in H. coronarium (72 g kg1 of DM) did not affect daily gain of lambs.160 Lascano et al.161 reported that the predominance of prodelphinidins in the extractable tannin fractions from different accessions of C. calothyrsus was associated with greater feed intake and digestion than when procyanidins were predominant.

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2 Wallace RJ, Antimicrobial properties of plant secondary metabolites. Proc Nutr Soc 63:621629 (2004). 3 Mueller-Harvey I, Unravelling the conundrum of tannins in animal nutrition and health. J Sci Food Agric 86:20102037 (2006). 4 Kamra DN, Patra AK, Chatterjee PN, Kumar R, Agarwal N and Chaudhary LC, Effect of plant extract on methanogenesis and microbial prole of the rumen of buffalo: a brief overview. Aust J Exp Agric 48:175178 (2008). 5 Hart KJ, Yanez-Ruiz DR, Duval SM, McEwan NR and Newbold CJ, Plant extracts to manipulate rumen fermentation. Anim Feed Sci Technol 147:835 (2008). 6 Waghorn GC, Benecial and detrimental effects of dietary condensed tannins for sustainable sheep and goat production progress and challenges. Anim Feed Sci Technol 147:116139 (2008). 7 Patra AK and Saxena J, Dietary phytochemicals as rumen modiers: a review of the effects on microbial populations. Anton van Leeuwen 96:363375 (2009). 8 Patra AK and Saxena J, A review of the effect and mode of action of saponins on microbial population and fermentation in the rumen and ruminant production. Nutr Res Rev 22:204219 (2009). 9 Kumar R and Vaithiyanathan S, Occurrence, nutritional signicance and effect on animal productivity of tannins in tree leaves. Anim Feed Sci Technol 30:2138 (1990). 10 Mangan JL, Nutritional effects of tannins in animal feeds. Nutr Res Rev 1:209231 (1988). 11 Aerts RJ, Barry TN and McNabb WC, Polyphenols and agriculture: benecial effects of proanthocyanidins in forages. Agric Ecosyst Environ 75:112 (1999). 12 Barry TN and McNabb WC, The implications of condensed tannins on the nutritive value of temperate forages fed to ruminants. Br J Nutr 81:263272 (1999). 13 McSweeney CS, Palmer B, McNeill DM and Krause DO, Microbial interactions with tannins: nutritional consequences for ruminants. Anim Feed Sci Technol 91:8393 (2001). 14 Min BR, Barry TN, Attwood GT and McNabb WC, The effect of condensed tannins on the nutrition and health of ruminants fed fresh temperate forages: a review. Anim Feed Sci Technol 106:319 (2003). 15 Haslam E, Plant Polyphenols. Cambridge University Press, Cambridge (1989). 16 Ferreira D, Brandt EV, Coetzee J and Malan E, Condensed tannins. Prog Chemist Org Nat Prod 77:2259 (1999). 17 Hagerman AE and Butler LG, Choosing appropriate methods and standards for assaying tannins. J Chem Ecol 11:15351544 (1989). 18 Hemingway RW, Reactions at the interavonoid bond of proanthocyanidins, in Chemistry and Signicance of Condensed Tannins, ed. by Hemingway RW and Karchesy JJ. Plenum Press, New York, pp. 265283 (1989). 19 Seigler DS, Plant Secondary Metabolism. Kluwer Academic Publishers, Dordrecht, p. 759 (1998). 20 Porter LJ, Hrstich LN and Chan BG, The conversion of procyanidins and prodelphinidins to cyanidin and delphinidin. Phytochemistry 25:223230 (1986). 21 Jones WT and Mangan JL, Complexes of the condensed tannins of sainfoin (Onobrychis viciifolia Scop.) with fraction 1 leaf protein and with submaxillary mucoprotein and their reversal by polyethelene glycol and pH. J Sci Food Agric 28:126136 (1977). 22 Terrill TH, Douglas GB, Foote AG, Purchas RW, Wilson GF and Barry TN, Effect of condensed tannins upon body growth and rumen metabolism in sheep grazing sulla (Hedysarum coronarium) and perennial pasture. J Agric Sci (Camb) 119:265273 (1992). 23 Van Soest PJ, Nutritional Ecology of the Ruminant, 2nd edition. Cornell University Press, Ithaca, NY, pp. 298, 346347 (1994). 24 Frutos P, Hervas G, Giraldez FJ and Mantecon AR, Review. Tannins and ruminant nutrition. Spanish J Agric Res 2:191202 (2004). 25 Foo LY, Newman R, Waghorn GC, McNabb WC and Ulyatt MJ, Proanthocyanidins from Lotus corniculatus. Phytochemistry 41:617624 (1996). 26 Foo LY, Lu Y, McNabb WC, Waghorn GC and Ulyatt MJ, The proanthocyanidins of Lotus pedunculatus. Phytochemistry 45:16891696 (1997). 27 Butler LG and Rogler JC, Biochemical mechanisms of the antinutritional effects of tannin, in Phenolic Compounds in Food and their Effects on Health. 1. Analysis, Occurrence and Chemistry, ed. by Ho C-T, Lee CY and Huang M-T. American Chemical Society, Washington, pp. 298304 (1992).

CONCLUSIONS
Tannins interact with proteins predominately via hydrogen bonds, forming tanninprotein complexes and thus preventing degradation of protein in the rumen. These tanninprotein complexes are dissociated in the abomasum, releasing protein. Tannins might also inhibit the growth of proteolytic bacteria, which can reduce proteolysis. These increase non-ammonia N ow in the intestine for absorption. Moderate concentrations (depending upon the type of tannins) of tannins in diets improve body weight and wool growth, milk yields and reproductive performance. However, these effects have not been consistently observed. These discrepancies among studies are attributed to the mode of tanninprotein interactions, which do not always work in an optimal mode depending upon the chemical structures of tannins and protein. While tannins may shift N metabolism from rumen to intestine, the effects of tannins on large intestinal protein metabolism and microbial populations are not known. Recently, inclusion of tannins in diets has been shown to enrich CLA content in meat and milk. Tannins can exert benecial effects environmentally by shifting N excretion from urine to faeces and decreasing methane output. Tannins lower methane production probably by directly inhibiting the activities of methanogenic archaea and/or reducing the bre digestion in the rumen. Not all types of tannins produce benecial nutritional and environmental responses. There is evidence that the structure of tannins may inuence physiological effects such as nitrogen metabolism, rumen microbial populations, intake and performance of animals, which has not been studied well in ruminant nutrition. The elucidation of structureactivity relationships would be required to obtain consistent benecial tannin effects in ruminants.

ACKNOWLEDGEMENT
The research grant provided by Indian Council of Agricultural Research, New Delhi is gratefully acknowledged.

REFERENCES
1 Barton MD, Antibiotic use in animal feed and its impact on human health. Nutr Res Rev 13:122 (2000).

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