5.8. The main detoxication route in galliforms may not be the liver

According to McArthur et al. (1991) there are at least six physiological mechanisms, which may be used for diminishing the effects of plant secondary compounds. Of these, formation of less reactive complexes, modification of the environment to inhibit reactions (for instance pH), and degradation, are taking place in the gut. Inactivated or degraded compounds may not have any harmful effects after absorption. If these defences fail, and absorption of these compounds occur, liver is the main site for addition of functional groups, and conjugation reactions (to change solubility). Kidneys, lungs, brain and intestinal mucosa contribute these processes.

Plant secondary compounds entail an effective detoxication mechanism or adaptation to certain levels of chemicals in herbivores. The biotransformation system – including both cytochrome P450 (CYP) enzymes and conjugation reactions, is considered to be the most important process against toxication in herbivores (Gonzales & Nebert 1990). The CYP enzyme system is closely related to feeding habits with specialised requirements for enzymatic detoxication of xenobiotics in the food (Walker et al. 1987, Walker & Ronis 1989, Fossi et al. 1995, Walker 1998, Dearing et al. 2000).

Intraspecific differences, that is, differences between wild and hand-reared birds of each species were found (IV). Wild capercaillies had significantly lower EROD and PROD activities than hand-reared birds, which may have reflected the decreasing effect of some phenolic compounds on the enzyme, at least EROD activity (Baer-Dubowska et al. 1998, Mimica-Dukic et al. 1999, Stupan et al. 2000). According to Lindén (1984b), Sjöberg and Lindén (1991), and Spidsø and Korsmo (1994) the pine needle diet of the capercaillie is rich in phenolic compounds (resins). Also in the grey partridge PROD activity was lower in wild birds in comparison to hand-reared birds. Naturally, delayed sampling could cause low enzyme activity values, but in this case it could not explain the whole decrease in the enzyme activity (IV). Wild and hand-reared birds of either of the species had similar COH activity. It is possible that secondary compounds present in the birds’ diets did not induce the activity of these certain CYP enzymes. However, bird species feeding on totally deviant diets may share similar hepatic biotransformation activities (Rivière et al. 1985).

EROD and PROD activities were similar in both species, and the only interspecific difference was found in COH (IV). The exact connection between the CYP enzymes used and secondary compounds in the diet of these birds still remains unknown, since studied CYP enzymes represented only a minor part of the large CYP enzyme family and did not completely reflect the detoxication capacity. Sampling may have affected the results, because it is shown that different parts of the liver show various enzyme activities (Gillette et al. 1972). The small number of birds used in this study may have had its impact on the results.

In the feeding trial with birds fed control, tannin and natural diets (V), the hepatic enzyme activity did not show any differences between diet groups with any of the substrates used. EROD activity seemed to be lower in the tannin group birds, but the difference was not significant. Enzymes used in this study are easily induced by several environmental toxins (e.g. Mattson et al. 1998), but natural substrates, like plant secondary compounds, may not induce these enzymes (H. Raunio, pers. comm.). Induction of EROD and PROD in polychlorobiphenyl-fed captive grey partridge males is reported (Abiola et al. 1989). According to Pelkonen et al. (2000) COH activity may be connected to coumarin-type alcaloids rather than tannins.

In addition to the hepatic detoxication enzymes, herbivores also have symbiotic micro-organisms in their caeca which may have an important role in the catabolism of secondary compounds (Hanssen 1979b, Hewitt et al. 1997). High CYP values are known from the duodenum of the grey partridge (Rivière 1980). This may reveal the main route for detoxication in birds to be the intestinal metabolism, and that the tannins are not absorbed from the intestine to blood circulation, thus not entering the liver for detoxication. Tetraonids probably detoxify resins in their caeca, where they are concentrated and excreted as energy-rich caecal droppings (Moss 1973, Pendergast & Boag 1971b). The increased length of the small intestine in tannin fed birds (V) may indicate an increased gastrointestinal detoxication activity.

Salivary tannin-binding proteins are found in mule deer Odocoileus hemionus, American black bears Ursus americanus (Robbins et al. 1991), root vole Microtus oeconomus (Juntheikki et al. 1996), and moose Alces alces (Juntheikki 1996), which may reduce fecal nitrogen losses (per unit of ingested tannin). However, such salivary proteins have not been found in birds. In animals which do not produce tannin-binding proteins, at least part of the condensed tannin are absorbed (McArthur et al. 1991). Galliform birds may also have a high resistance to secondary compounds, as suggested for the greater snow goose Anser caerulescens atlantica (Gauthier & Bédard 1990).