- Effects of condensed tannins on browsers and grazers
|Last update: April 12, 2012 11:31:49 AM|
Effects of condensed tannins on browsers and grazers
P G Marais
Grootfontein Agricultural Development Institute
Private Bag X529, Middelburg EC. 5900
Tanniniferous trees and shrubs are of importance in animal production because they can provide significant protein supplements. Unfortunately the amount of tannins that they contain varies widely and unpredictably. Their effects on animals range from beneficial to toxic, including death. The toxic or anti-nutritional effects may be exacerbated in times of stress when a very large proportion of the diet is tanniniferous.
Recent work in the area of plant-herbivore interactions has focused on the inhibitory effects of condensed tannins on protein and fibre digestion in mammals. Tannins have previously been classified as a quantitative plant defence, which reduce the digestibility of nutrients following their ingestion by herbivores (Feeny, 1976; Rhodes & Cates 1976). It is well known that the defensive nature of tannins as digestion inhibitors or toxins is dependent on the molecular characteristics of the tannin as it interacts with the physiological capability of the animal.
Digestion inhibitors, such as tannins, act within an animal's digestive tract by binding with the substrate to be digested (usually proteins, but also carbohydrates), inhibiting digestive enzymes, or being antimicrobial (Scalbert, 1991).
One effective strategy for dealing with the digestion inhibiting properties of condensed tannins has recently been elucidated in browsing mammals. These herbivores (e.g. goats), which generally consume a wide variety of tannin-containing trees and shrubs, are known to produce proline-rich proteins (PRP) in their saliva. These proteins complex with tannins in the mouth of the herbivore and then pass through the animal's gut intact, thereby effectively neutralizing some of the tannins' adverse effects. In addition, PRP being rich in non-essential amino acids are excreted instead of essential amino acids from dietary proteins, providing a qualitative nitrogen saving.
Grazing mammals (e.g. sheep), on the other hand, typically ingest a relatively tannin-free diet of grasses and forbs and appear to be incapable of synthesizing PRP. It is commonly thought that because these animals have evolved with virtually tannin-free diets, they therefore have little reason for production of PRP. But, what happens when grazers are subjected to an increase in dietary tannin levels, as might be the case when an area becomes overgrazed and animals are forced to include more tannin-containing plants in their diets? If they are incapable of PRP synthesis, are there other strategies available to them for dealing not only with the digestion-inhibiting properties of tannins, but their toxicity levels as well?
Effects of tannins on digestion and metabolism
There are several possible explanations for the anti-nutritional effects of condensed tannins. As outlined by Fahey & Jung (1989), 1) tannins depress food intake, 2) tannins complex with dietary proteins or other dietary components, 3) tannins complex with digestive enzymes, thus interfering with normal digestion, 4) tannins complex with endogenous protein, resulting in a drain on the nitrogen supply and on the amino acid supply in particular, 5) tannins complex with or injure parts of the alimentary tract and 6) tannins or their hydrolysis products are absorbed and have a toxic effect elsewhere in the body.
Tannins, because of their protein-binding properties, are known to be strongly astringent.
Astringency is the sensation caused by the formation of complexes between tannins and salivary glycoproteins. This astringency appears to be the major cause of reduced food intake in mammalian herbivores. There is some controversy, however, over whether reduced food intake is a result of the toxic nature of tannins. When tannins complex with protein in an animal's gut, they are believed to be responsible not only for growth depression, but also for low protein digestibility and increased faecal nitrogen concentrations. Thus, once they have been consumed, their adverse effects, once again, seem to be related to their binding of dietary protein.
There is evidence to suggest that enzymatic proteins, as well as other endogenous proteins, comprise a considerable portion of excreted nitrogen when animals are fed tannins (Fahey & Jung, 1989). When endogenous proteins are lost in this manner, the animal may incur a deficiency in one or more essential amino acids.
Condensed tannins are known to inhibit several digestive enzymes, including proteases, pectinases, amylases, cellulases and lipases. There are many factors, which may influence the extent of digestive enzyme inhibition by tannins.
Defensive strategies of browsers and grazers
Because tannins have such a wide array of effects on herbivores, it is difficult to predict with any certainty how a particular tannin-containing forage will affect an animal without first understanding something about the characteristics of the tannin (e.g. molecular size and configuration) and the adaptations that different animals possess for neutralizing or metabolising them (Clausen et al., 1990).
Which strategy an herbivore uses to cope with plant secondary compounds depends to a great extent on the animal's behaviour and its physiological capability (McArthur et al., 1992). In addition to behavioural adaptations, several physiological mechanisms are available to browsers and grazers for reducing the activity of plant secondary compounds (McArthur et al., 1992). They include the following: 1) formation of a less reactive complex, 2) modification of the environment to inhibit reactions, 3) degradation, 4) addition of functional groups, 5) conjugation to change solubility and 6) alteration of metabolic rate. McArthur et al., (1992) considered the first three listed above, as the "first line of defence".
According to McArthur et al., (1992), the first line of defence takes place in the gut. If tannins can be inactivated or degraded to harmless compounds, then the toxic effects that occur after absorption are avoided
First line defensive strategies
The toxic effects of tannin compounds may be inactivated by the formation of non-covalent complexes with other compounds in the gut. The resulting complex must be less reactive or less readily absorbed across the gut wall. Because of the reduced absorption, the complex may then be excreted in the faeces. Although complex formation is effective in the prevention of tannin absorption it can also be considered anti-nutritional when tannins bind with dietary protein, which then make dietary protein unavailable to the herbivore.
Tannins are known to form such complexes (both soluble and insoluble) by binding with dietary and endogenous proteins. The salivary proline-rich proteins produced by many browsers are considered one such defensive strategy against these secondary metabolites. The tannin-protein complex (at least in goats) is thought to be stable throughout the entire digestive tract (Austin et al., 1989).
Degradation of tannin
Animal enzymes and gut micro-organisms potentially play an important role in deactivating tannins in an animal's digestive tract. Bacteria are capable of modifying a broader range of compounds than are mammals, and can thus be significant in determining the fate and toxicity of these plant defensive compounds. However, time of exposure can be a key factor in how well this defence works, and it can take up to several months of exposure to secondary compounds before gut microbes have adapted to utilizing them (McArthur et al., 1992).
Consumption of plant secondary compounds by mammalian herbivores has resulted in the evolution of several different behavioural and physiological responses. According to McArthur et al., (1992), the primary determinants of which mechanisms are used are dependent on the feeding niche of the animal and features of its gut structure. These authors divide herbivorous mammals into 4 groups, based on the feeding niche that they occupy: grazer, intermediate mixed feeder, generalist browser, and specialist browser. Each group reflects differences in levels of consumption of plant secondary compounds and in strategies for dealing with such compounds.
This classification scheme represents a continuum of animals, with grazers on the one hand to specialist browsers on the other end, which consume, almost exclusively, plants containing high levels of plant secondary metabolites. Examples of grazers include domestic cows and sheep, which feed mainly on grasses and forbs, whereas, specialist browsers are herbivores such as koalas and greater gliders, which feed heavily on the tannin-rich leaves of Eucalyptus trees.
McArthur et al., (1992) further suggests that the occurrence of salivary PRP is somewhat predictable, based on the feeding niche of the animal. Grazers do not apparently possess this adaptation. A much broader survey of PRP production in herbivorous mammals is an obvious need in this area of research!
Gut structure influences the pathways and sites of tannin metabolism (McArthur et al., 1992). For example, animals, which possess a foregut, such as ruminants, maintain microflora in their rumens, which degrade some secondary compounds to water-soluble, readily excreted products. This degradation of secondary compounds by microbes in the foregut could also potentially be harmful, where after degradation, soluble tannins could then perhaps be absorbed across the gut wall.
Understanding how tannins function in plant-herbivore interactions depends to a great extent on our knowledge not only of the chemistry of these polyphenolic compounds, but also of the strategies that herbivores possess for dealing with these substances. In mammals, which are capable of PRP synthesis, ingested condensed tannin is complexed in the gut and then excreted in the faeces. Tannins, in this case, may somewhat reduce feed intake and digestibility, but can be considered as more of a quantitative defence according to the definitions of Feeny (1976) and Rhodes & Cates (1976). On the other hand, in animals, which do not produce PRP, at least some part of the tannin may be absorbed, potentially yielding toxic effects.
Much remains to be learned about tannins and their interactions with mammalian herbivores. Indeed, it may not even be possible to classify tannins as a qualitative or quantitative defence. Instead, what type of defence they act as may depend more on what type of herbivore is ingesting them.
Austin, P. J., Suchar, L.A., Robbins, C.T., & Hagerman, A.E., 1989. Tannin-binding proteins in saliva of deer and their absence in saliva of sheep and cattle. J. Chem Ecol. 15:1335-1339
Clausen, T. P., Provenza, F.D., Burritt, P.A., Reichardt, P.B. & Bryant, J.P., 1990. Ecological implications of condensed tannin structure: a case study. J. Chem. Ecol. 16:2381-2391
Fahey, G. C. & Jung, H.G., 1989. Phenolic compounds in forages and fibrous feedstuffs. In: P. R. Cheeke (ed). Toxicants of plant origin. Vol. IV Phenolics. CRC Press, Inc. Florida. p. 123-190
Feeny, P. R., 1976. Plant apparency and chemical defence. Recent Adv. Phytochem. 10:1-40
McArthur, C., Hagerman, A.E. & Robbins, C. T., 1992. Physiological strategies of mammalian herbivores against plant defences. In: R. T. Palo and C. T. Robbins (eds). Plant defences against mammalian herbivory. CRC Press Inc., Florida. p 103-114
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