A Comparison of mucosal surface area and villous histology in small intestines of the Brazilian free‐tailed bat (Tadarida brasiliensis) and the mouse (Mus musculus)

Abstract

Studies on birds have led to the hypothesis that increased intestinal absorption between enterocytes (paracellular) evolved as a compensation for smaller intestinal size in fliers, which was perhaps selected to minimize the mass of digesta carried. This hypothesis predicts that bats will also exhibit relatively reduced intestinal size and high paracellular absorption, compared with nonflying mammals. Published studies on three bat species indicate relatively high paracellular absorption. One mechanism for increasing paracellular absorption per cm2 small intestine (SI) is increased number of tight junctions (TJs) across which paracellular absorption occurs. To our knowledge, we provide the first comparative analysis of enterocyte size and number in flying and nonflying mammals. Intestines of insectivorous bats Tadarida brasiliensis were compared with Mus musculus using hematoxylin and eosin staining method. Bats had shorter and narrower SIs than mice, and after correction for body size difference by normalizing to mass3/4, the bats had 40% less nominal surface area than the mouse, as predicted. Villous enhancement of surface area was 90% greater in the bat than in the mouse, mainly because of longer villi and a greater density of villi in bat intestines. Bat and mouse were similar in enterocyte diameter. Bats exceeded mice by 54.4% in villous area per cm length SI and by 95% in number of enterocytes per cm2 of the nominal surface area of the SI. Therefore, an increased density of TJs per cm2 SI may be a mechanistic explanation that helps to understand the high paracellular absorption observed in bats compared to nonflying mammals.

Quantification of the neurons of myenteric plexus of the bat molossus rufus

“…Regarding the studies on the bats' digestive tube, they stand out for their histology (Makanya et al 2001, Gadelha-Alves et al 2008, Strobel et al 2015, Zhang et al 2015 and microbiology (Ingala et al 2018, Sens Junior et al 2018. However, Barry-Jr (1976) already emphasized the little research about the different segments of this system, including the intestine to wild mammals, a real fact still today, once that the studies on ENS are widely disseminated to rodents (Karaosmanoglu et al 1996, Tan et al 2008, Luesma et al 2013, Grundmann et al 2015, Kulkarni et al 2017 and more recently to primates (Noorian et al 2011), but in terms of other groups of wild mammals, not employed in experimental models, the absence of data is notorious.…”

Digestive Adaptations of Aerial Lifestyles

“…Birds and bats sometimes have more villous amplification than nonflyers (57,87,123) and sometimes have smaller enterocytes (87). Both properties would lead to more tight junctions per nominal surface area.…”

“…Both properties would lead to more tight junctions per nominal surface area. However, due to their smaller small intestine, birds and bats still often have fewer total enterocytes, and presumably tight junctions, summed over the entire small intestine in studies that demonstrate higher paracellular nutrient absorption in the flying species (57,87,123). Furthermore, the greater villous amplification in flying species is often not enough to explain their greater paracellular probe absorption in in situ perfusion…”

Improved capacity to evaluate changes in intestinal mucosal surface area using mathematical modeling

“…The surface area enlargement factor (SEF) allows for the conversion of a two‐dimensional serosal length into a three‐dimensional mucosal area, using the mathematical model described and used previously to calculate MSA (Kisielinski et al, ; Zhang et al, ). The formula used to calculate the SEF is shown in Figure .…”