- Changing perceptions of the effect of plant tannins on nutrient supply in the ruminant
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Changing perceptions of the effect of plant tannins on nutrient supply in the ruminant
Dr P G Marais
Grootfontein Agricultural Development Institute
Private Bag X529, Middelburg EC
The level of animal production achieved in any environment is generally related to the quantity, quality and continuity of supply of feed available throughout the year. Trees and shrubs are of importance in animal production because they provide significant protein supplements (12 – 30%), but unfortunately the amounts of tannins that they contain vary widely and largely and their effects on animals range from beneficial to toxicity and death. Tannins are tentatively classified into two classes: hydrolysable (HT) and condensed tannins (CT). These tannins are widely distributed in the leaves of trees and shrubs, but occur in the leaves and stems of only a small number of specialised non-woody forage legume plants (Barry, 1989). The toxic or anti-nutritional effects may be exacerbated in times of stress when a very large proportion of the diet is tanniniferous. Increased knowledge about tannins has contributed to different definitions of tannins throught the years. These definitions have tended to be either too narrow or too broad (Zucker, 1983). With a better understanding of tannin properties, the mechanism of tannin action and proper management of forages, browses could become an invaluable source of protein for strategic supplementation.
Effects of tannins on nutritive value of ruminant feeds
The ability of tannins to form strong complexes with proteins is the most important aspect of their anti-nutritional effects. The effects of CT, such as inhibition of feed intake and digestion by ruminants, are usually ascribed to their ability to bind to proteins (D'Mello, 1992). The strength of the tannin-protein complexes (TPC) depends on characteristics of both the tannin and protein (Haslam, 1989). Tannins bind with at least four groups of proteins in the ruminant: dietary proteins, salivary proteins, endogenous enzymes and gut microbes including microbial enzymes (Hagerman & Butler, 1981).
The HT and CT differ in their nutritional significance and toxic effects, but both precipitate proteins. While CT is not readily degraded in the gut, HT undergoes microbial and acid hydrolysis with the release of simpler phenolics. These are absorbed and can cause toxicity (Murdiati et al., 1992). While CT reduces forage quality, the HT causes poisoning in animals if sufficient quantities are consumed (Zhu et al., 1995). In contrast, CT have detrimental nutritional effects such as reducing feed intake, reducing feed digestibility and increasing faecal N excretion (Reed & Soller, 1987). On the other hand, CT can be of benefit in the prevention of bloat (Jones et al., 1973) and in the protection of feed protein against degradation in the rumen (Barry et al., 1986).
In ruminants consuming high quality fresh forages, a high proportion of the protein ingested may be degraded in the rumen. The portion of dietary protein that escapes to the small intestine for absorption may be inadequate to meet the total metabolisable protein needs for high levels of animal production (Douglas et al., 1995)
In temperate legumes with a high digestibility and high rumen degradability of feed protein, metabolisable protein requirements of high producing animals may not always be met. In such conditions, low levels of CT may be beneficial by reducing rumen degradability of feed protein (Terrill et al., 1992b). Conversely, with excess CT in the diet there can be a complete absence of soluble protein in the rumen, which reduces microbial protein synthesis and metabolisable protein supply to the animal (Jones & Mangan, 1977).
Nitrogen absorption and amino acid supply to the small intestine
CT can reduce the degradation of proteins in the rumen and increase essential amino acid absorption in ruminants fed these types of diets (Barry & McNabb, 1999), provided they are not in excess.
An increase in the flow of metabolisable protein or essential amino acids to the small intestine has been observed in animals grazing forages of high CT content compared to those grazing a low CT diet (Wang et al., 1994; McNabb et al., 1993; Waghorn et al., 1990; Barry & Manley, 1986; John & Lancashire, 1981). Benefits from feeding forages of high CT will be evident only where there is adequate rumen degradable N to meet microbial needs (Leng, 1992) and where the increase in bypass protein supply is not offset by a decrease in microbial protein flow to the small intestine.
Whilst higher concentrations of CT have been associated with increased N retention in sheep fed a high CT diet (Barry et al., 1986; Harrison et al., 1973), high CT concentrations in a number of browse species, when fed as supplements to straw, have been associated with reduced N retention (Ben Salem et al., 1997; Reed et al., 1990; Ebong, 1995; Woodward & Reed, 1997). These divergent results may be due to the differences in soluble N or digestibility of the basal diets, as well as actual content and composition of CT. Increased faecal N and reduced urinary N have been shown to correspond with increasing levels of CT in the diet (Woodward & Reed, 1997).
Phenols have a varying effect on N retention and intake, depending on the basal diet, including dietary CP content (Holechek et al., 1990). An investigation of a range of forage species (including fresh and conserved pastures and shrubs) indicated that rumen ammonia concentrations were associated with the N content of forage in an exponential manner. Ruminal fermentation of the tannin-containing forages resulted in much lower ammonia concentrations than ruminal fermentation of forages without tannins (Meissner et al., 1993).
The extent of carbohydrate digestion is dependent on the characteristics of the feeds, including both the inherent degradability and rate of fermentation, and the rate of feed intake and passage (Pitt et al., 1999). If protein resists degradation or diets are deficient in protein, microbial growth in the rumen is sub-optimal, and this in turn leads to retarded carbohydrate breakdown (McDonald et al., 1995).
Feeding of high-tannin forage to ruminants can induce a deficiency of rumen-degradable N, thus indirectly impairing the fermentation of structural carbohydrates (D'Mello, 1992). CT not bound to protein can inhibit the fermentation of structural carbohydrates in the rumen by forming indigestible complexes with cell wall carbohydrates, rendering them undegradable. It can form complexes with microbial enzymes, rendering them inactive (Gamble et al., 1996).
Although the majority (i.e. 70-95%) of CT in a number of browse species is soluble, it is the high content of bound CT in some species with which their low digestibility is primarily associated. Jackson et al. (1996) emphasised the need to consider not only tannin levels but also digestibility of the plant. Similarly, Lowry et al. (1996) reported that it is important to distinguish between high-phenolic plants with a composition that is otherwise of high feed quality and high-phenolic plants that are also highly fibrous.
Palatability and voluntary feed intake
In general, there is an inverse relationship between tannin concentration in browse sources and voluntary feed intake by herbivores (Kumar & Vaithiyanathan, 1990). The negative effects of tannins on palatability and digestibility in ruminants are multiple (Kumar & Vaithiyanathan, 1990). They include: (i) reduction in protein availability due to binding of food proteins and inactivation of enzymes in the digestive tract, (ii) astringency caused by the interaction of tannins with salivary protein and oral mucosa, and (iii) gut irritation and systemic toxicity. All of the aversive effects can reduce forage palatability.
Palatability has been thought to be associated with CT concentration (Jones et al., 1976) due to astringency (Kumar & Singh, 1984). Astringency is the sensation caused by the formation of complexes between tannins and salivary glycoproteins (Butter et al., 1999). This may increase salivation and decrease palatability (Reed, 1995).
The general conclusion appears to be that low dry matter intake is principally associated with the inhibitory effects of the high CT on digestion (Reed et al., 1990; Degen et al., 1995; Chriyaa et al., 1997; Degen et al., 1997; Odenyo et al., 1997), rather than palatability associated with CT.
Polyethylene glycol as means to neutralise the detrimental effects of tannins
Polyethylene glycol (PEG) is a polymer that can bind tannins irreversibly, and its presence reduces the formation of protein-tannin complexes (Jones & Mangan, 1977). Thus, supplementation with PEG has been used to alleviate the negative effects of tannins on livestock (Landau et al., 2000). Although, amongst various tannin-complexing agents investigated, PEG of molecular weight 6000 was the most effective in binding to tannins at near neutral pH values.
Inactivation of tannins through PEG increased availability of nutrients and decreased microbial inhibition, which in turn increased degradability of nutrients leading to higher animal performance. Besides concentration of tannins, their nature is another factor that would also influence response of animals to PEG incorporation. A diet containing 1.8% condensed tannins through L. pedunculatus caused significant reduction in the levels of rumen ammonia and short-chain fatty acids and reduced nitrogen digestibility, whereas the same level of condensed tannins (1.8%) from L. corniculatus had lesser effects (Waghorn & Shelton, 1997). The effect of PEG also depends on the level of proteins in the diet. Higher the level of proteins, lesser is the effect of PEG (Makkar & Becker, 1996).
A thorough review of literature on the effects of PEG on livestock (Getachew et al., 1998) revealed that sheep or goats have been used in these studies, and that the amount of PEG incorporated into the diets varied from 3 to 120 g per day, with varying responses. Supplementing sheep and goats, fed C. siliqua leaves, with 25 g of PEG per day tannins seems to be the optimal amount in terms of cost-benefit response under Israeli conditions (Silanikove et al., 1994). Studies to know the in vivo optimum tannin:PEG ratio for ‘near-complete’ inactivation of tannin-rich feedstuffs, by taking into account the tannin level and activity and intake of tannins are needed.
Worth mentioning here is the higher efficiency of microbial protein synthesis in vitro on incorporating PEG in smaller portions in dispersed manner compared to the total of all portions of PEG at one time (Getachew et al., 2001), and higher microbial protein synthesis in vivo observed by measuring excretion of urinary purine derivatives on feeding PEG through ‘lick blocks’ (Ben Salem et al., 2001;). This approach of incorporating PEG in the ‘lick blocks’ is likely to decrease the cost of PEG treatment through lower PEG requirement (Getachew et al., 2001) and possible self-regulation of PEG intake. Indeed, recent studies showed that sheep and goats can self-regulate the intake of PEG (Villalba & Provenza, 2001).
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