Tannins: toxic and antinutritional effects

Tannins act as a defense mechanism in plants against pathogens, herbivores and hostile environmental conditions. Generally, tannins induce a negative response when consumed. These effects can be instantaneous like astrigency or a bitter or unpleasant taste or can have a delayed response related to antinutritional/toxic effects.

This section will cover the effect of tannins on:

• Intake
• Feed digestibility
• Toxicity to microorganisms
• Toxicity to ruminants
• Toxicity to monogastric
• Animals' defense mechanisms

Tannins negatively affect an animal's feed intake, feed digestibility, and efficiency of production. These effects vary depending on the content and type of tannin ingested and on theanimal's tolerance, which in turn is dependent on characteristics such as type of digestive tract, feeding behavior, body size, and detoxification mechanisms.

Sites of action of tannins :

• Oral cavity - mastication ruptures the plant cell tissue and exposes proteins and carbohydrates to tannins.
• Rumen and gastrointestinal tract lumen - unbound tannins complex dietary proteins and metabolic proteins (e.g. bacteria, enzymes, epithelial cells).

Intake

Tannins may reduce intake by decreasing palatability and by negatively affecting digestion.

• Palatability is reduced because tannins are astringent. Astringency is the sensation caused by the formation of complexes between tannins and salivary glycoproteins.
  • Low palatability depresses feed intake and, thus, animal productivity.
• Digestibility reduction (see following section) negatively influences intake because of the filling effect associated with undigested feedstuff.
• Several studies have reported higher feed intakes and weight gains when tannin-free diets were compared to tannin-containing ones.
  • Some caution must be taken when interpreting these results. In many trials, commercial tannins sources were used. These types of tannins are usually more effective at lowering feed intakes than naturally-occurring tannins.
  • Another likely problem in many trials is that often only extractable tannins are measured and insoluble tannins are not quantified. However, insoluble tannins may have equal or greater biological activity than those that are more easily extracted.
  • When naturally-occurring tannins are used, these tannins do not always reduce intake. In some trials, tannin-rich diets were eaten in equal or larger amounts than low or free tannin diets.
• The form in which the forage is fed may influence how tannins affect feed intake. Forages rich in tannins are eaten in larger amounts when field dried rather than fresh frozen. Indeed, drying reduces the solubility of tannins and, hence, reduces their ability to complex proteins (tannins become more polimerized, resulting in a lower number of free hydroxyls available for binding the proteins).
• Intake in animal diets rich in tannins can be increased by using a compound with a high affinity for tannins, like PEG (polyethylene glycol).
  • PEG has a higher affinity to tannins than do proteins.
  • PEG can be sprayed on the forages or added in the diet and is fairly inexpensive.
  • PEG utilization can increase feed palatability and digestibility and result in higher animal productivity.
• Feed intake may also be decreased by low molecular weight phenolics. They predominate during the early stages of plant growth and are then converted to oligomers and finally to polymers (tannins) when the plant mature. These low MW phenolics are absorbed into the body and exhibit systemic effects such as alteration of physiological systems, increased energy requirements due to detoxification, and subsequent growth rate reduction.

Feed digestibility

Usually PAs are not absorbed through the digestive tract. Instead, free tannins and complexed forms remain in the rumen, decreasing protein and plant cell wall digestibility.

Carbohydrate digestibility

• Several studies have shown that tannins decrease organic matter and fiber digestion.
• The lower digestibility is the result of the interaction of tannins with cellulase enzymes and rumen bacteria.
• In some cases, lower fiber digestibility can be the result of a shortage of ruminally fermented nitrogen due to the complexation of proteins by tannins.
• Field drying and treatments with PEG are able to limit these negative effects.
• In some cases, lower digestibility was compensated by higher protein outflow from the rumen.

Protein digestibility

• In in vivo studies, protein digestibility is greatly reduced when tanniniferous feeds are part of the diet.
• Plants high in PAs often have proteins linked tightly to the plant cell wall (neutral-detergent insoluble nitrogen, NDIN) and lignin (acid detergent lignin, ADL) components, and, thus, may show negative digestion coefficients when ingested.
  • After ingestion, PAs may also form detergent insoluble tannin-protein complexes with proteins they encounter. These two factors may cause the amount of NDIN and ADL excreted in the feces to exceedthe amount ingested.
• When dietary content of tannins increases, fecal nitrogen excretion increases due to lower digestibility of nitrogen fractions and formation of tannin-protein complexes.
• However, despite the decrease in apparent nitrogen digestibility, nitrogen retention does not always decrease with increasing tannin concentration in the diet. In many cases, nitrogen retention increases as a result of decreased urinary excretion.
• The effect of tannins on protein digestibility of a specific feed can be estimated using Lucas's test (Van Soest, 1994, page 360).
  • If protein digestibility is not affected by tannins, proteins behave as a uniform fraction, with a regression coefficient (true digestibility) equal to or larger than 0.88, with a negative intercept(estimate of metabolic endogenous nitrogen, usually about 0.5% of dry matter intake or smaller) and with a low standard error.
  • However, if protein digestibility is affected by tannins, the proteins will behave as a non-uniform fraction, with a regression coefficient (true digestibility) smaller than 0.88, and with a larger negative intercept and a higher standard error
• Tannin solubility plays a role in determining a tannin's efficiency in binding proteins and/or fiber.
  • If the ratio of soluble to insoluble tannins is high, then protein digestibility is affected more than fiber digestibility.
  • If the same ratio is low, fiber digestibility is the most affected.

Toxicity to microorganisms

Tannin toxicity to rumen microorganisms has been described for several bacteria species such as Streptococcus bovis, Butyvibrio fibrosolvens, Fibrobacter succinogenes, Prevotella ruminicola, and Ruminobacter amylophilis.

• Three mechanisms of toxicity have been identified
  • enzyme inhibition and substrate deprivation,
  • action on membranes,
  • metal ion deprivation.
• Tannins induce changes in morphology of several species of ruminal bacteria.
• Microrganism defense mechanisms involve
• • secretion of binding polymers,
  • synthesis of tannin-resistant enzymes,
  • biodegradation of tannins (peculiarity of some recently discovered bacteria that are able to tolerate high levels of PA).

Toxicity to ruminants

Hydrolizable tannins

Hydrolizable tannins are toxic to ruminants. Tannin toxicity from HTs may occur in animals fed oak (Quercus spp.) and several tropical tree legumes (e.g. Terminalia oblongata and Clidema hirta)

Microbial metabolism and gastric digestion convert HTs into absorbable low molecular weight metabolites. Some of these compounds are toxic.

• The major lesions associated with HT poisoning are hemorrhagic gastroenteritis, necrosis of the liver, and kidney damage with proximal tuberal necrosis,
• High mortality and morbidity were observed in sheep and cattle fed oaks and other tree species with more than 20% HT.

Protanthocyanidins

Toxicity from PA is difficult to separate from their effects on the digestion of proteins and carbohydrates.

• PAs are not absorbed by the digestive tract,
• PAs may damage the mucosa of the gastrointestinal tract, decreasing the absorption of nutrients,
• PAs may reduce the absorption of essential aminoacids. The most susceptible amino acids are methionine and lysine.
  • Decreased methionine availability could increase the toxicity of cyanogenic glycosides, because methionine is involved in the detoxification of cyanide via methylation to thiocyanate.

Toxicity to monogastrics

Animals fed diets with a level of tannins under 5% experience

• depressed growth rates,
• low protein utilization,
• damage to the mucosal lining of the digestive tract,
• alteration in the excretion of certain cations, and
• increased excretion of proteins and essential amino acids.

In poultry, small quantities of tannins in the diet cause adverse effects

• levels from 0.5 to 2.0% can cause depression in growth and egg production,
• levels from 3 to 7% can cause death.

In swine, similar harmful effects of tannins have been found.

The addition of additional proteins or amino acids may alleviate the antinutritional effects of tannins.

Levels of tannins above 5% of the diet are often lethal.

Animal defense mechanisms

Hoatzin: a ruminant-like bird that eats a lot of tannin-rich leaves

Some insects consume leaves with high levels of tannins. They are able to adapt to tannins using several available mechanisms

• alkaline gut pH,
• presence of surfactants to decrease affinity between ingested tannins and protein,
• presence of peritrophic membranes that absorb tannins and are then excreted in the feces.

Many tannin-consuming animals secrete a tannin-binding protein (mucin) in their saliva.

• Tannin-binding capacity of salivary mucin is directly related to its proline content. Advantages in using salivary proline-rich proteins (PRPs) to inactivate tannins are
  • PRPs inactivate tannins to a greater extent than do dietary proteins; this results in reduced fecal nitrogen losses,
  • PRPs contain non specific nitrogen and nonessential amino acids; this makes them more convenient for an animal to exploit rather than using up valuable dietary protein.
• There are species differences in the amount of PRP that different species produce to bind tannins
  • Ability to tolerate tannins - deer> goat> sheep> cattle
  • Consumption of high tannin diets stimulates the development of the salivary glands to permit more PRP production,
  • Some researchers claim that sheep and cattle do not have any PRPs.