Integrative Zoology 2006; 2 : 67-69
doi: 10.1111/j.1749-4877.2006.00015.x
ORIGINAL ARTICLE
Metabolism of carbohydrate in alimentary tract of reindeer in winter Tatyana I. KOCHAN Institute of Physiology, Komi Science Center, Ural Branch of Russian Academy of Sciences, Syktyvkar, Pervomayskaya, Russia
Abstract The study was conducted on six reindeers in December. It was established that concentration of reducing sugars in the chyme of jejunum increases substantially (6 times in comparison with abomasum), whereas concentration cellulose, on the contrary, decreases (4.5 times). The maximal increase of monosaccharides in the small intestine testifies to formation of metabolic fund of sugars in this part of the alimentary tract due to high degree of polysaccharides hydrolysis of exogenous, as well as endogenous, microbial formation. Obtained data assume that the need of the reindeer for glucose is provided for not only by gluconeogenesis as it was considered before, but also by absorption of monosaccharides from the alimentary tract. Key words: alimentary tract, blood glucose, carbohydrate metabolism, reindeers.
INTRODUCTION In winter, the main food source for the reindeer is lichens with high carbohydrate content (72-95% of dry matter) and extremely low content of nitrogen and mineral substances (Borozdin et al. 1979; Kochanov et al. 1981; White et al. 1984; Staaland & White 1991). However, it was established (Kochanov et al. 1981), that notwithstanding the disbalance of nutrients in lichen, the alimentary tract of reindeer is adapted to high digestibility of lichen organic matter (80%), cellulose and nitrogen-free extractives (8090%), whereas home ruminants (cattle and sheep) digest only 65-72% of organic matter and 50-55% of cellulose of lichen (Kochanov et al. 1981). A considerable amount (40% of dry matter) of lichen is presented by lichenin, cellulosesimilar homopolysaccharide ( -1,4 and -1,3 glucan). It is
Correspondence: Tatyana I. Kochan, Institute of Physiology, Komi Science Center, Ural Branch of Russian Academy of Sciences, Syktyvkar 167982, Pervomayskaya, 50, Russia. Email:
[email protected]
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possible that high adoption of lichen in reindeer is due to the action of specific rumen microorganisms, which produce enzyme lichenase. Moreover, as was established in the chronic experiments that Kochan (1987) conducted on reindeer with intestinal anastomosis, the small intestine plays an essential role in assimilation of carbohydrates. There is little knowledge obtained on processes of digestion and the mechanism of adaptation to low-nutritive lichens. Therefore the objective of this research was to study the carbohydrates concentration in the contents of all parts of alimentary tract of reindeer in winter and to estimate the change of carbohydrates composition of the chyme during its moving along the gastroenteric path.
MATERIALS AND METHODS The investigations were conducted on female reindeers (n = 6) with average body weight 80 ± 2 kg, in December. Before the animals were slaughtered, their blood had been taken from the jugular vein to determine glucose concentration. After the slaughter, the content of different sections of their alimentary tract (rumen, reticulum, omasum,
T. I. Kochan
Table 1 The content of dry matter and water (per cent of wet matter) and carbohydrates (per cent of dry matter) in different parts of alimentary tract in reindeer in winter Part of alimentary tract
Dry matter
Water
Cellulose
Rumen Reticulum
14.3±2.1 14.4±2.3
85.7±2.1 85.6±2.3
Omasum
22.6±1.7
Abomasum Duodenum
10.8±1.2 10.2±0.6
Jejunum, 0-4 m Jejunum, 4-11m Jejunum, 11-22 m
Reducing sugars Aldoses
Ketoses
Sum of sugars
11.3±1.0 11.4±1.4
0.64±0.12 0.63±0.15
0.93±0.17 1.06±0.23
1.57±0.29 1.69±0.37
77.4±1.7
14.0±1.1
0.34±0.07
0.50±0.1
0.84±0.16
89.2±1.2 89.8±0.6
12.7±1.0 3.0±0.6
0.41±0.06 1.39±0.25
0.63±0.06 1.92±0.19
1.04±0.12 3.51±0.55
14.9±0.9
85.1±0.9
2.9±0.6
3.13±0.22
2.8±0.12
6.06±0.31
15.8±1.3 13.6±0.9
84.2±1.3 86.4±0.9
3.8±1.0 5.8±0.7
2.36±0.33 1.39±0.25
2.54±0.28 1.29±0.22
4.99±0.56 2.71±0.48
Ileum
15.2±1.5
84.8±1.4
10.7±0.7
0.39±0.02
0.46±0.06
0.85±0.06
Caecum Large colon
16.4±0.5 16.7±0.1
83.6±0.5 83.3±1.0
11.6±1.2 12.1±0.6
0.78±0.13 0.44±0.06
0.34±0.07 0.38±0.09
1.12±0.14 0.82±0.08
Small colon
23.4±0.2
76.6±1.6
12.0±0.6
0.45±0.04
0.46±0.05
0.91±0.06
Rectum
30.9±0.1
69.1±1.5
11.1±0.8
0.37±0.02
0.38±0.05
0.75±0.04
abomasum, duodenum, jejunum, ileum, cecum, large colon, small colon, rectum) was measured, and concentration of cellulose and reducing sugars was analyzed within the chyme. Jejunum content was analyzed in the proximal, middle and distal sections (0-4 m; 4-11 m; >11 m). The data were statistically analyzed using Student’s ttest.
RESULTS The investigations showed that the concentration of cellulose and sugars in dry matter of rumen and reticulum chyme was similar (Table 1) and it did not differ from the concentration of these carbohydrates (12.9 and 1.9% respectively) in lichen. In the omasum the cellulose level rose 23%, in comparison with the rumen and the reticulum, while the concentration of reducing sugars (aldoses and ketoses) decreased twofold (P < 0.05). The cellulose concentration decreased essentially (4.3-fold, P < 0.001) and the level of sugars, in contrast, increased (3.4-fold, P < 0.001) progressively on the way from the abomasum to the duodenum. Towards the middle part of the jejunum, the concentration of cellulose and sugars attained extreme values (minimum and maximum). The content of cellulose rose (3.8-fold as compared to minimum value, P < 0.001) and sugars became lower (7-fold in comparasion with the maximum value, P < 0.001) in the distal small intestine. The concentration of carbohydrates changed insignificantly through the large intestine. Gross weight of wet chyme in the alimentary tract in
reindeer equaled 10.5 kg, 77.5% of which was in the rumen and only 6.6% in the small intestine and 10.7% in the large intestine. Dry matter of chyme was distributed in the alimentary tract approximately in the same proportion, with some decrease in the rumen and in the small intestine, and an increase in the large intestine. The content of dry matter was 2.4-fold higher in the large intestine than in the small intestine, whereas the length of the large intestine was half that of the small intestine. The total amount of cellulose in the alimentary tract was 170.7 g, 76% of which was in the rumen, 3% in the small intestine, and 16% in the large intestine. The total content of reducing sugars was 26.7 g, 75% of this contained in the rumen, 13% in the small intestine, and 8% in the large intestine. The glucose concentration in the blood of the reindeer was high (4.2 ± 0.5 mmol L-1). On the basis of data by Kurilov and Krotkova (1971), indicating that volume of blood in ruminant animals comprises approximately 8% of liveweight, it was calculated that the glucose content in the total volume of the reindeer blood was 4.8 g. Comparison of this value with the quantity of reducing sugars in the small intestine and whole digestive tract indicates that absorption of sugars from alimentary tract plays an important role in the maintenance of high glucose level in blood in reindeer.
DISCUSSION It is known (Kurilov & Krotkova 1971) that the requirement of carbohydrates in ruminants is determined not only
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Reindeer carbohydrate metabolism
by the requirements of the animal itself, but also by the requirements of rumen microorganisms. Enzymes, secreted by bacteria and protozoa, bring about the chemical breakdown of complex carbohydrates to simple sugars, and further, to volatile fatty acids, carbon dioxide and methane. The simple sugars produced at the first stage of carbohydrate digestion in the rumen are rarely detectable in rumen liquor, because they are immediately taken up and metabolized intracellularly by microorganisms. Therefore, it is maintained that in ruminants, as compared to monogastric animals, a very small amount of endogenic glucose is absorbed from the alimentary tract. The glucose requirement of the animal itself is provided for by gluconeogenesis in the liver from such precursors as propionic and lactic acids, and glucogenic amino acids and glycerol. However, together with gluconeogenesis, there is an additional source of glucose. The microorganisms of ruminants also possess polysaccharides produced by secondstage microbial processing, which are hydrolyzed by intestine enzymes of the host organism. The present data shows that the content of cellulose in the rumen of reindeer exceeds considerably the content of reducing sugars. But in comparison with the intake, which had been established in the previous studies of reindeer having analogous liveweight (Kochanov & Kochan 1987), the total content of cellulose in the rumen is lower (33%) and that of sugars is higher (16%) than their consumption. This testifies to intensive hydrolysis of lichen polysaccharides. The drawback of this comparison is that in conditions of quick experiment it is impossible to determine the daily amount of chyme. Nevertheless, even without calculation of chyme evacuation it is clear that a large amount of sugars, formed from polysaccharides during rumen metabolism, is not fermented to volatile fatty acids in reindeer. Assumption of a lower acid production in reindeer rumen in winter has been confirmed by Staaland and White (1991). Therefore, it is thought that a considerable amount of carbohydrate may be absorbed directly from the rumen as glucose in winter. The highest reduction of cellulose concentration in the duodenum chyme and in the proximal jejunum, in comparison with the abomasum, can be explained by dilution, which occurs a result of intensive secretion of endogenous substances into the intestine cavity. At the same time, maximal increase of sugar level in these conditions testifies to a high degree of hydrolysis of polysaccharides of exogenous, as well as of endogenous microbial formation. The increase of cellulose concentration in the chyme of the mid jejunum and the lowering of sugars are the result of domination of nutrient absorption processes. The data indicate that high adoption of lichen polysaccharides is due not only to adap-
© 2006 ISZS, Blackwell Publishing and IOZ/CAS
tive possibilities of digestion in the rumen, but also to adaptation of enzyme systems of the small intestine to a more complete hydrolysis of the polysaccharides. The earlier chronic experiments, conducted on reindeer with intestinal anastomosis (Kochan 1987), showed that, on a lichen diet, the mean daily amount of sugars that pass through certain parts of the small intestine, is 8.7 g (0-4 m), 7.3 g (10 m) and 5.5 g (distal end). These data confirm the significant role of the small intestine in adoption of carbohydrates in reindeer. Comparison of the gross sugar amount formed in the small intestine, with the volume of blood glucose, indicates that in the small intestine of reindeer there is a metabolic pool of sugars formed, which is sufficient for maintaining a high glycemic level. An addition to this is the rumen sugars, a large quantity of which, due to decrease of their fermentation, can be absorbed into the blood. Thus, it is thought that the requirement of glucose in reindeer in winter is supplied not only by gluconeogenesis, as is generally believed, but also by a considerable absorption of sugars from the alimentary tract.
REFERENCES Borozdin EK, Zabrodin VA, Vostryakov PN, D’jachenko NO, Kryuchkov VV, Andreev VN (1979). Severnoe olenevodstvo. Kolos, Moskva 286 (in Russian). Kochan TI (1987). Usvoenie uglevodov v pishchevaritelnom trakte severnykh oleney. Vliyanie ekologicheskikh faktorov na produktivnost’ dikikh zhivotnykh v ekosistemakh Evropeiskogo severo-vostoka SSSR: Trudy Komi nauchny tsentr AN SSSR, 89. Syktyvkar. pp. 154–62. (in Russian.) Kochanov NE, Ivanova GM, Weber AE, Symakov AF (1981). Obmen veshchestv u dikikh zhvachnykh zhyvotnykh (severnye oleni i losi). Nauka, Leningrad, pp. 252. (in Russian.) Kochanov NE, Kochan TI (1987). [Sezonnye izmeneniya uglevodnogo pitaniya u severnykh oleney.] Ecology 1, 50–5. (in Russian.) Kurilov NV, Krotkova AP (1971). Phyziologiya i biokhimiya pishchevareniya zhvachnykh. Kolos, Moskva, pp. 432. (in Russian.) Staaland H (1991). Influence of foraging ecology on alimentary size and function of Svalbard reindeer. Canadian Journal of Zoology 69, 1326–34. White RG, Jacobsen E, Staaland H (1984). Secretion and absorption of nutrients in the alimentary tract of reindeer fed lichens or concentrates during the winter. Canadian Journal of Zoology 62, 2364–76.
