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First published online June 11, 2007
Journal of Experimental Biology 210, 2033-2045 (2007)
Published by The Company of Biologists 2007
doi: 10.1242/jeb.000976

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Physiological and morphological responses to feeding in broad-nosed caiman (Caiman latirostris)

J. Matthias Starck^1,*, Ariovaldo P. Cruz-Neto² and Augusto Shinya Abe^2,3

¹ Department of Biology, University of Munich (LMU), Munich, Germany
² Department of Zoology, State University of São Paulo, Rio Claro, Brazil
³ CAUNESP, State University of São Paulo, Rio Claro, Brazil

View larger version (107K): [in this window] [in a new window]   Fig. 1. Anatomy and ultrasonography of broad nosed caiman. (A) Chequerboard pattern of ventral scales and marks for application of the ultrasound scanner head (B) Partial situs of the body cavity. Black bars in A and B indicate scanner head position resulting in the images in C, D and E; (C) duodenum and liver (D). (C–E) Ultrasound anatomy of the duodenum (C), distal small intestine (D), and liver and gall bladder (E). Ultrasound anatomy of the liver and gall bladder. Abbreviations: ab, adipose tissue body; dd, duodenum; gb, gall bladder; L, liver; m, ventral muscles; si, distal small intestine; sto, stomach. The scanner head was positioned on the ventral scales of the caiman, thus in the ultrasonographs (C–E) ventral is at the top and dorsal is at the bottom. Green lines in C–E indicate the morphometric measurements. Scale bars, 1 cm (C–E).

View larger version (6K): [in this window] [in a new window]   Fig. 2. Changes in the thickness of the mucosa in the duodenum as measured by ultrasonography. Black symbols with negative error bars represent values from caimans that were first feed then fasted, white symbols with positive error bars are values from caimans fasted for 3 months then feed a single meal. Values are least square means ± s.e.m. derived from RM ANCOVA; for raw data see Table 1. Arrows indicate feeding events for each experimental group.

View larger version (6K): [in this window] [in a new window]   Fig. 3. Changes in the thickness of the mucosa in the distal small intestine as measured by ultrasonography. Black symbols with negative error bars represent values from caimans that were first feed then fasted, white symbols with positive error bars are values from caimans fasted for 3 months then feed a single meal. Values are least square means ± s.e.m. derived from RM ANCOVA; for raw data see Table 1. Arrows indicate feeding events for each experimental group.

View larger version (6K): [in this window] [in a new window]   Fig. 4. Changes of the size of the liver as measured by ultrasonography. Black symbols with negative error bars represent values from caimans that were first feed then fasted, white symbols with positive error bars are values from caimans fasted for 3 months then feed a single meal. Values are least square means ± s.e.m. derived from RM ANCOVA; for raw data see Table 1. Arrows indicate feeding events for each experimental group.

View larger version (138K): [in this window] [in a new window]   Fig. 5. Light microscopy and transmission electron microscopy of the duodenal mucosa epithelium of digesting caimans. Enterocytes are filled with lipid droplets and arranged as a single layered high prismatic epithelium. (A) Low power light micrograph of a villus showing the typical arrangement of lipid filled enterocytes with a well developed brush border and a large capillary in the connective tissue core of the villus. (B) High power light micrograph of the mucosa epithelium. Note the dense layer of lyphocytes and a large mast cell below the epithelium. (C) High power light micrograph of the tip of a villus with necrotic cells. Necrotic cells are enlarged as compared with healthy enterocytes and show different degrees of lysis of the cell membranes as well as the nuclei. (D) Low power transmission electron micrograph. Note the dense distribution of mitochondria and lipid droplets. (E) High power transmission electron micrograph of the brush border with pinocytotic pits at the basis of microvilli (arrows). bb, brush border; c, capillary; eec, enteroendocrine cell; iel, intraepithelial lymphocyte; l, lymphocytes; la, lacteal; lp, lipid droplet; m, mitochondria; mc, mast cell; mv, microvilli; n, nucleus of enterocytes; ne, necrotic enterocytes.

View larger version (138K): [in this window] [in a new window]   Fig. 6. Light microscopy and transmission electron microscopy of the duodenal mucosa epithelium of fasting caimans. The enterocytes are narrow, contain no lipid droplets, and are arranged as a pseudostratified epithelium. The brush border is barely visible. The connective tissue cores of the villi are broader and more condensed than in digesting caimans. (A) Low power light micrograph, showing the arrangement of arrangement of the enterocytes as typical pseudostratified epithelium. Note the aggregation of lymphocytes at the base of the middle villus. (B) High power light micrograph of the mucosa epithelium (same magnification as Fig. 5B). (C) Transmission electron micrograph of the mucosa epithelium with enterocytes and one enteroendocrine cell, the lumen of the gut contains an accumulation of cellular debris. (D) Segment of the cell membrane of two adjoining enterocytes showing folds of spare membrane (arrows). (E) Microvilli of an enterocyte exfoliating membrane vesicles from the tip of the microvilli. (F) Bifurcating microvilli. (G) Microvilli of the brush border disintegration, i.e. swollen tips and formation of membrane vesicles. bb, brush border; cd, cellular debris in lumen of gut; eec, enteroendocrine cell; gc, goblet cell; iel, intraepithelial lymphocyte; l, lymphocytes; m, mitochondria; mc, mast cell; mv, microvilli; mvs, membrane vesicles; n, nucleus of enterocytes; smc, smooth muscle cell.

View larger version (4K): [in this window] [in a new window]   Fig. 7. Changes in the absorptive surface of the duodenum (circles) and the small intestine (squares) in feeding (filled symbols) and fasting (open symbols) caimans. Values are means ± s.d. from N=5 animals. Differences between the feeding and fasting condition are highly significant (see text for details of statistics).

View larger version (130K): [in this window] [in a new window]   Fig. 8. Light micrographs of the liver of feeding and fasting caimans. (A) Low power micrograph of the liver of a feeding caiman. (B) High power micrograph of the liver tubules of a feeding caiman. (C) Low power micrograph of the liver of a fasting caiman. (D) High power micrograph of the liver tubules of a fasting caiman. bc, bile canaliculus; bd, bile duct; h, hepatocytes; ha, branch of the hepatic artery; k, Kupffer cell; pv, branch of the portal vein; s, sinusoid.

View larger version (22K): [in this window] [in a new window]   Fig. 9. Oxygen consumption of caimans (N=8) for 2 days before feeding and 9 days after feeding. Feeding was around noon of day 0 as indicated by the grey bar. The plotted curves were derived by fitting data to a log normal 4 parameter model. (A) Continuous measurements over the entire experimental period. Values are means of eight individuals; each animal was assessed for 10 min during an 80-min interval. (B) Daily mean O2 derived from data in A. Values are means ± s.d. from all measurement intervals per day for eight individuals. Different letters denote significant difference according to Tukey's HSD post-hoc test for comparisons of multiple means; <0.05. The grey shaded area under the curve represents SDA; the vertical bar indicates interruption of the continuous measurements for feeding.