Morphological bases for intestinal paracellular absorption in bats and rodents

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 microanatomical 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 presented 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 similar 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 explanation for understanding the high paracellular absorption observed in bats compared to nonflying mammals. K E Y W O R D Sbats, enterocytes, nutrient absorption, rodents, small intestine surface area

Alpha-Ketoglutarate: An Effective Feed Supplement in Improving Bone Metabolism and Muscle Quality of Laying Hens: A Preliminary Study

“…Villus length and crypt width determine the intestinal absorptive surface and nutrient absorption. A surface area of the small intestine is a key determinant of the absorptive capacity [61]. Moreover, in the assessment of the intestinal response to various diets, the determination of the villus to crypt ratio is also effective [62].…”

Small nutrient molecules in fruit fuel efficient digestion and mutualism with plants in frugivorous bats

“…In conclusion, contrary to our initial hypothesis, short intestines and rapid digestion do not limit the digestive efficiency of frugivorous bats. This may have as much to do with the nutritional composition of fruit, and with the microanatomy of the intestine 56 , as with the gross anatomy of the gastrointestinal tract. Our results support the previously known fact that fruit of Piper species is rich in soluble sugars.…”

“…The absorption of small nutrient molecules, such as simple sugars, free amino acids, and peptides, occurs directly through the paracellular and transcellular pathways 57,58 . The first is important in bats 56,59 . Food rich in small nutrient molecules should result in a fast and high assimilation, even with short intestines, as we observed.…”

“…A high concentration of free amino acids and soluble sugars in fruit is likely to be important for this mutualism. The probable effects, not necessarily in evolutionary order, are as follows: (1) by rewarding the frugivores with fruit containing simple nutrient molecules, plants avoid the greater metabolic costs of producing complex nutrient molecules 63 , thus becoming capable of allocating more resources to vegetative growth and to competition with other plants; (2) the foraging efficiency of frugivores increases by being rewarded with fruit containing simple nutrient molecules that can be readily assimilated through paracellular and transcellular absorption 29,56 ; (3) the more efficient that frugivores are as foragers, the more of them that plants will be able to attract and sustain with a given biomass of fruit; (4) rapid assimilation of nutrients allows the frugivores to increase their feeding rates to acquire sufficient amounts of less abundant nutrients, such as free amino acids; (5) increased feeding rates augment fruit removal from plants, hence seed dispersal; (6) a high foraging efficiently is crucial for the survival of frugivores during climate-driven shortages of fruit 64,65 .…”

Plasticidade digestiva, metabolismo energético e composição corporal no morcego Anoura caudifer (Phyllostomidae: Glossophaginae)

“…Apesar de existirem poucos estudos com A. caudifer, considera-se que a absorção intestinal paracelular seja um processo essencial nos morcegos, onde a glicose pode ser rapidamente absorvida e utilizada como combustível para o voo (Voigt e Speakman, 2007;Brun et al, 2019). Por outro lado, problemas decorrentes de hiperglicemia podem ser superados, nessa espécie, com a ação da insulina, além do exercício corporal que impede o estabelecimento da condição patológica de uma hiperglicemia crônica Castro et al, 2021).…”