A stereological comparison of villous and microvillous surfaces in small intestines of frugivorous and entomophagous bats: species, inter-individual and craniocaudal differences

Abstract

The extents of functional surfaces (villi, microvilli) have been estimated at different longitudinal sites, and in the entire small intestine, for three species of bats belonging to two feeding groups: insect- and fruit-eaters. In all species, surface areas and other structural quantities tended to be greatest at more cranial sites and to decline caudally. The entomophagous bat (Miniopterus inflatus) had a mean body mass (coefficient of variation) of 8.9 g (5 %) and a mean intestinal length of 20 cm (6 %). The surface area of the basic intestinal tube (primary mucosa) was 9.1cm2 (10%) but this was amplified to 48cm2 (13 %) by villi and to 0.13m2 (20 %) by microvilli. The total number of microvilli per intestine was 4´1011 (20 %). The average microvillus had a diameter of 89 nm (10 %), a length of 1.1 mm (22%) and a membrane surface area of 0.32 mm2 (31 %). In two species of fruit bats (Epomophorus wahlbergi and Lisonycteris angolensis), body masses were greater and intestines longer, the values being 76.0 g (18 %) and 76.9 g (4 %), and 73 cm (16 %) and 72 cm (7 %), respectively. Surface areas were also greater, amounting to 76cm2 (26 %) and 45cm2 (8 %) for the primary mucosa, 547cm2 (29 %) and 314cm2 (16 %) for villi and 2.7m2 (23 %) and 1.5m2 (18 %) for microvilli. An increase in the number of microvilli, 33´1011 (19 %) and 15´1011 (24 %) per intestine, contributed to the more extensive surface area but there were concomitant changes in the dimensions of microvilli. Mean diameters were 94 nm (8 %) and 111 nm (4 %), and mean lengths were 2.8 mm (12 %) and 2.9 mm (10 %), respectively. Thus, an increase in the surface area of the average microvillus to 0.83 mm2 (12 %) and 1.02 mm2 (11%) also contributed to the greater total surface area of microvilli. The lifestyle-related differences in total microvillous surface areas persisted when structural quantities were normalised for the differences in body masses. The values for total microvillous surface area were 148cm2 g-1 (20 %) in the entomophagous bat, 355cm2 g-1 (20 %) in E. wahlbergi and 192cm2 g-1 (17 %) in L. angolensis. This was true despite the fact that the insecteater possessed a greater length of intestine per unit of body mass: 22mmg-1 (8 %) versus 9–10mmg-1 (9–10%) for the fruit-eaters.