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Structural flexibility of the small intestine and liver of garter snakes in response to feeding and fasting

J. Matthias Starck^* and Kathleen Beese

Institute of Systematic Zoology and Evolutionary Biology, University of Jena, Erbertstrasse 1, D-07743 Jena, Germany

View larger version (26K): [in a new window]   Fig. 1. Relative body mass changes of garter snakes under different feeding regimes. (A) Fasting snakes; (B) snakes fed every other day; (C) snakes fed once a week. In B and C, the body mass reported includes the mass of the ingested prey. Body mass is expressed relative to the mass of the individual on the day before the experiment started.

View larger version (65K): [in a new window]   Fig. 2. Transcutaneous ultrasonographs of the small intestine of (A) fasting garter snakes and (B) snakes 2 days after feeding. Both figures are parasagittal images of the small intestine (the top of the image is cranial, the bottom is caudal, left is ventral, right is dorsal). The ventral scales and the dorsal aorta were used as morphological landmarks. The thickness of the mucosa was measured as the distance between the two dark lines of the tunica muscularis. v, ventral scales; a, dorsal aorta; si, small intestine mucosa; the arrows indicate the tunica muscularis; *imaging artifacts. Scale, major dimensions, 10 mm.

View larger version (28K): [in a new window]   Fig. 3. Flexible response of the small intestinal mucosa to feeding measured from ultrasonographs. For comparison, multiple measurements of each individual were averaged by individual and day. Values are means ± S.D. from the four snakes in each group. Dotted lines indicate feeding events. (A) Fasting snakes, open symbols; (B) snakes fed every other day, black symbols; grey symbols are for animals that were shedding their skin and did not feed; (C) snakes fed once a week, grey symbols.

View larger version (57K): [in a new window]   Fig. 4. Transcutaneous ultrasonographs of the liver of (A) fasting garter snakes and (B) snakes 2 days after feeding. Both figures are cross-sectional images through the snake. Left is ventral, right is dorsal. 1, liver; p, hepatic portal vein, v, hepatic vein; s, stomach; *imaging artifacts. Scale, major dimensions, 10 mm.

View larger version (26K): [in a new window]   Fig. 5. Flexible response of the liver to feeding measured from ultrasonographs. Multiple measurements of each individual were averaged by individual and day; to account for size differences among individuals, measurements are expressed relative to the size (cross-sectional diameter) of the liver of each individual on the day before the experiment started. Values are means ± S.D. from the four snakes in each group. Dotted lines indicate feeding events. (A) Fasting snakes, open symbols; (B) snakes fed every other day, black symbols; grey symbols are for snakes that did not feed; (C) snakes fed once a week, grey symbols.

View larger version (141K): [in a new window]   Fig. 6. Histology of the mucosal epithelium of digesting snakes 2 days after feeding. (A) Methacrylate-embedded section of the small intestine; Methylene Blue/Thionine stain. Scale bar, 50 µm. The mucosal epithelium is a single-layered columnar epithelium. (B) Methacrylateembedded section of the small intestine; Methylene Blue/Thionine stain. Scale bar, 25 µm. Note the large lacteals, blood-filled capillaries and lipid droplets in the enterocytes. (C) Low-power electron micrograph of enterocytes filled with lipid droplets. Scale bar, 2.5 µm. (D) High-power electron micrograph of microvilli. Scale bar, 0.5 µm.

View larger version (131K): [in a new window]   Fig. 7. Histology of the mucosal epithelium of fasting snakes. (A) Methacrylate-embedded section of the small intestine; Methylene Blue/Thionine stain. Scale bar, 50µm (same magnification as Fig. 6A). The mucosal epithelium is a typical pseudostratified transitional epithelium. Note that no lacteals or lipid droplets can be seen and the capillaries are small and empty. (B) Low-power electron micrograph of enterocytes. An amoeboid cell can be seen in the lower half of the image (asterisk). Scale bar, 2µm. (C) High-power electron micrograph of microvilli. Compare with Fig. 6D, which was taken at the same magnification. Scale bar, 0.5µm. (D) High-power electron micrograph of enterocyte membrane forming typical folds (arrow) of spare membrane. Scale bar, 0.4µm. (E) High-power electron micrograph showing extensive folding (arrow) of the basal membrane in the relaxed state. Scale bar, 1.7µm.

View larger version (126K): [in a new window]   Fig. 8. Histology of the mucosal epithelium of snakes fed once a week. (A) Methacrylate-embedded section of the small intestine; Methylene Blue/Thionine stain. Scale bar, 50µm (same magnification as Figs 6A and 7A). The mucosal epithelium has an intermediate configuration compared with Figs 6A and 7A with two layers of nuclei, few lipid droplets, reduced lacteals and reduced numbers of capillaries. (B) Histology as in A (same magnification as Fig. 6B). Scale bar, 25µm. (C) Low-power electron micrograph of transitional epithelium. Note the small lipid droplets (arrows) in the apical part of the enterocytes. Scale bar, 5 µm. (D) High-power electron micrograph of microvilli. Compare with Fig. 6D, which was taken at same magnification. Scale bar, 0.5µm.

View larger version (133K): [in a new window]   Fig. 9. Histology of the liver. (A) Digesting snake (2 days after feeding) Methacrylate-embedded section of the liver; Methylene Blue/Thionine stain. Scale bar, 50 µm. Note the many lipid droplets (stars) in the hepatocytes. (B) Digesting snake, low-power electron micrograph of hepatocytes loaded with lipid droplets and glycogen deposits. Scale bar, 4 µm. Arrows, glycogen deposits; stars k, lipid droplet. (C) Fasting snake. Methacrylate-embedded section of the liver; Methylene Blue/Thionine stain. Scale bar, 50 µm. (D) Fasting snake, low-power electron micrograph of hepatocytes. Note that no lipid droplets can be seen in the hepatocytes and that glycogen deposits are depleted. Scale bar, 4 µm. Arrows, glycogen deposits; star, lipid droplet. (E) The liver from a group 3 snake (fed once a week). Methacrylate-embedded section of the liver; Methylene Blue/Thionine stain. Scale bar, 50 µm. Star, lipid droplet. (F) Low-power electron micrograph of hepatocytes from a group 3 snake. Histology is intermediate and some lipid droplets can be seen in the hepatocytes together with glycogen deposits. Scale bar, 4 µm; arrows, glycogen deposits; star, lipid droplet.