RESEARCH ARTICLE Morphological bases for intestinal paracellular absorption in bats and rodents Antonio Brun 1,3 | Guido Fernández Marinone 2 | Edwin R. Price 4 | Lucas A. Nell 5 | Beatriz M. V. Simões 6 | Alexandre Castellar 6 | Manuel Gontero-Fourcade 1,2 | Ariovaldo P. Cruz-Neto 6 | William H. Karasov 3 | Enrique Caviedes-Vidal 1,2 1 Instituto Multidisciplinario de Investigaciones Biológicas de San Luis, Consejo Nacional de Investigaciones Científicas y Técnicas, San Luis, Argentina 2 Departamento de Bioquímica y Ciencias Biológicas, Facultad de Química, Bioquímica y Farmacia. Universidad Nacional de San Luis, San Luis, Argentina 3 Department of Forest and Wildlife Ecology, University of Wisconsin–Madison, Madison, Wisconsin 4 Department of Biological Sciences, University of North Texas, Denton, Texas 5 Department of Integrative Biology, University of Wisconsin–Madison, Madison, Wisconsin 6 Departamento de Zoologia, Instituto de Biociências, Universidade Estadual Paulista “Julio de Mesquita Filho” Rio Claro, São Paulo, Brazil Correspondence William H. Karasov, Department of Forest and Wildlife Ecology, University of Wisconsin- Madison, 1630 Linden Drive, Madison, WI 53706. Email: wkarasov@wisc.edu Funding information Argentina Consejo Nacional de Investigaciones Científicas y Técnicas, Grant/Award Number: PIP834; Argentina Universidad Nacional de San Luis; Brazil CNPq, Grant/Award Number: 470128/2011-9; Fundaçao de Amparo a Pesquisa do Estado de Sao Paulo, Grant/Award Number: 2012/04610-5; U.S. National Science Foundation, Grant/Award Number: IOS- 1025886 Abstract Flying mammals present unique intestinal adaptations, such as lower intestinal surface area than nonflying mammals, and they compensate for this with higher paracellular absorption of glucose. There is no consensus about the mechanistic bases for this physiological phenomenon. The surface area of the small intestine is a key determinant of the absorptive capacity by both the transcellular and the paracellular pathways; thus, information about intestinal surface area and micro- anatomical structure can help explain differences among species in absorptive capacity. In order to elucidate a possible mechanism for the high paracellular nutrient absorption in bats, we performed a comparative analysis of intestinal villi architecture and enterocyte size and number in microchiropterans and rodents. We collected data from intestines of six bat species and five rodent species using hematoxylin and eosin staining and histological measurements. For the analysis we added measurements from published studies employing similar methodology, making in total a comparison of nine species each of rodents and bats. Bats pres- ented shorter intestines than rodents. After correction for body size differences, bats had ~41% less nominal surface area (NSA) than rodents. Villous enhancement of surface area (SEF) was ~64% greater in bats than in rodents, mainly because of longer villi and a greater density of villi in bat intestines. Both taxa exhibited simi- lar enterocyte diameter. Bats exceeded rodents by ~103% in enterocyte density per cm 2 NSA, but they do not significantly differ in total number of enterocytes per whole animal. In addition, there is a correlation between SEF and clearance per cm 2 NSA of L-arabinose, a nonactively transported paracellular probe. We infer that an increased enterocyte density per cm 2 NSA corresponds to increased density of tight junctions per cm 2 NSA, which provides a partial mechanistic expla- nation for understanding the high paracellular absorption observed in bats com- pared to nonflying mammals. KEYWORDS bats, enterocytes, nutrient absorption, rodents, small intestine surface area Received: 3 May 2019 Revised: 19 June 2019 Accepted: 26 June 2019 DOI: 10.1002/jmor.21037 Journal of Morphology. 2019;1–11. wileyonlinelibrary.com/journal/jmor © 2019 Wiley Periodicals, Inc. 1